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. However, restricted species samples and inconsistent methodologies are limiting comparative phylogenetic studies. By combining original data with published literature reports, we assembled data on hand preferences for standardized object manipulation in 1,806 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 significant population-level handedness to be notably rare. Species-level direction of manual lateralization was largely uniform among non-human primates and neither correlated with phylogeny nor with any of the selected biological predictors. 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, especially 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 displayed by our species.

Cerebral Polymorphisms for Lateralisation: Modelling the Genetic and Phenotypic Architectures of Multiple Functional Modules

“…Meguerditchian et al [414], in an analysis similar to that for marsupials, found that ecology rather than phylogeny seemed important, arboreal species showing a left-hand preference for bimanual coordinated tasks, whereas terrestrial species tended to be right-handed. The more extensive study of 38 species of anthropoid primates by Caspar et al [415] found little phylogenetic influence on direction of handedness, suggesting "unique selective pressures gave rise to . .…”

Hand preferences in coordinated bimanual tasks in non-human primates: a systematic review and meta-analysis

“…Firstly, this study reviews the state of the art of manual laterality studies in non-human primates with those tasks (coordinated bimanual actions) that are potentially more sensitive and precise for measuring manual preferences. To date, we have not found any published review or meta-analysis comparable to this one, except for a recent pre-print that includes some of our database and incorporates new data not included in the present meta-analysis (Caspar et al, 2021). Secondly, it highlights the great heterogeneity of procedures, assessments and sample sizes used in laterality research in nonhuman primates.…”

“…It would be especially relevant in future studies to test whether hand preference is linked to phylogeny and species-level predictors (e.g. vocal repertoire, dietary breadth, group size, terrestriality, home range or feeding budget) through phylogenetic analysis (Caspar et al, 2021). That is, to identify the possible factors that drive or influence this trait along the phylogenetic tree.…”

Age, but not hand preference, is related to personality traits in common marmosets (Callithrix jacchus)

“…Yet, population-level handedness (i.e. the tendency of the majority of the population toward using a specific hand as is known in humans) is extremely rare in animals [ 17 ]. Instead, vast individual variation in direction (i.e.…”

“…asymmetry in hemispheric functions, has been hypothesized as one of the possible proximate neurophysiological mechanisms that maintain personality variation [12,13]. Brain lateralization is expressed as a preference for using the contralateral part of the body and is often measured either as a limb preference [14][15][16][17][18], eye dominance [19,20] or tail and body orientation [12,21,22]. Brain lateralization is present both in vertebrates and invertebrates (reviewed in [23,24]), and it provides various benefits in terms of enhanced cognition, social cohesion and better predator detection while foraging [25][26][27], thus directly affecting an individual's survival.…”