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.

Pronounced right-handedness is a universal trait among extant human populations (Coren and Porac, 1977; Raymond and Pontier, 2004; Faurie et al., 2005) and might be an ancient attribute of the genus Homo (Toth, 1985; Lozano et al., 2017). Whereas a significant expression of manual lateralization at population level is not exclusive to humans, the universal proportion of approximately 85–95% right-handers in our species appears to be an unmatched extreme among primates (Meguerditchian et al., 2013). Furthermore, individual humans tend to be strongly handed with ambiguous hand preferences being extremely rare (Cochet and Vauclair, 2012), which is also unusual when compared to many other primate lineages (Westergaard and Suomi, 1996; Hopkins et al., 2011). Therefore, both strength and direction of population-level manual lateralization in humans are widely considered to be remarkable.

Handedness is a behavioral consequence of functional asymmetries in the brain (Amunts et al., 1996; Häberling and Corballis, 2016; Sha et al., 2021). Accordingly, right-handedness results from unilateral specializations in the left hemisphere and vice versa. In anthropoid primates, which encompass monkeys, apes, and humans, asymmetries of the precentral gyrus in the primary motor cortex show a particular association with hand preference at the individual level (Yousry et al., 1997; Phillips and Sherwood, 2005; Dadda et al., 2006; Sha et al., 2021). Nevertheless, the proximate reasons for the expression of individual manual lateralization in humans and other anthropoids, including its genetic basis and the influence of brain areas located outside of the motor cortex, are by no means fully understood (Rogers, 2009; Hopkins et al., 2013a; Ocklenburg et al., 2014; Schmitz et al., 2017a; Richards et al., 2021). For this paper, however, we exclusively focus on the evolutionary underpinnings of population-level hand preferences.

The origins of pronounced population-level right-handedness in the human lineage have traditionally been linked to the emergence of complex communication mediated by manual gestures and language, which are also predominantly processed in the left hemisphere (Corballis, 1991; Annett, 2002; Meguerditchian et al., 2013; Ocklenburg et al., 2014; Prieur et al., 2019). However, current evidence suggests that manual and language lateralization are not nearly as tightly correlated as once believed and functional ties between these phenomena remain unidentified (Fitch and Braccini, 2013; Ocklenburg et al., 2014; Schmitz et al., 2017b). It has also been established that various non-human primates show significant asymmetries in hand use at the individual and population level in a variety of tasks, including manual communicative gestures and bimanual actions (MacNeilage, 2007; Hopkins et al., 2013a; Meguerditchian et al., 2013; Regaiolli et al., 2016). Nevertheless, reports of significant population-level biases are largely confined to a comparatively small number of species and the distribution of individuals across hand preference categories is always far more balanced than in humans. For instance, olive baboons (Papio anubis), Western gorillas (Gorilla gorilla), and chimpanzees (Pan troglodytes) have all been reported to show a significant population-level right-hand bias for bimanual manipulation but the portion of right-handers among these species is only around 50% (Vauclair et al., 2005; Hopkins et al., 2011 – note that this skew is significant due to a notable portion of ambipreferent individuals among these species). Still, it is essential to discern what underlies these comparatively weak population-level hand preference patterns that emerged across the primate order to unravel the origins of pronounced right-handedness in our species (MacNeilage, 2007).

The most influential conjecture to explain how primate hand preference patterns evolved is the postural origins hypothesis (POH) (MacNeilage et al., 1987; MacNeilage, 2007). Considering galagos as models, the POH assumes that hypothetical insectivorous primate ancestors exhibited a right-hand bias to support their body on vertical substrates, while the left-hand specialized for fast grasping movements, the so-called ballistic reaching (Ward, 1998). Based on this, the POH predicts that with the emergence of anthropoid primates, which exhibit arboreal quadrupedalism and more refined digit control, the right hand became adopted to manipulate objects during foraging (MacNeilage et al., 1987). Hence, it proposes that all anthropoids share a right-hand bias for manipulation, which would find its most extreme expression in humans (MacNeilage, 2007; MacNeilage et al., 1987). In the anatomically less derived strepsirrhines, the left hand is instead expected to be dominant (MacNeilage, 2007). However, the POH has been drastically modified in more recent studies (Hopkins et al., 2011; Meguerditchian et al., 2013; Morino et al., 2017). The novel interpretation proposes (in conflict with the original POH) that arboreal monkeys and apes should display a left-hand bias for manipulation. Their right hand would provide the necessary postural support, retaining the hypothesized ancestral primate pattern laid out by MacNeilage et al., 1987. Terrestrial lineages, however, would no longer be bound to reserve the right hand for posture stabilization and are expected to evolve right-hand preferences for fine motor skills, eventually giving rise to the human condition. Hence, the novel POH expects that left-handedness is prevalent in arboreal groups, while a preponderance of right-handedness should be restricted to terrestrial primate species (Meguerditchian et al., 2013). In contrast, the original POH expects to find a right-handedness trend in all anthropoids, regardless of their ecology. Both versions of the POH exclusively rely on correlational evidence from behavioral studies on hand preferences in different primate groups.

In addition to these considerations, it has been prominently proposed that foraging-related extractive tool use facilitated the evolution of hand preferences in humans to allow for more efficient object handling (Kimura, 1979; Frost, 1980). By now, this idea has also been extended to non-human primates that habitually use tools (Cashmore et al., 2008; Prieur et al., 2019). Moreover, neuroanatomical studies demonstrated that the expression of overall neural lateralization and hemispheric independence positively correlates with absolute brain size in primates (Rilling and Insel, 1999; Karolis et al., 2019; Ardesch et al., 2021). Such a scaling relation was already hypothesized by Ringo et al., 1994, and implies that the strength of individual handedness could also be tied to absolute brain size (Hopkins, 2013a; the concept does, however, not concern the direction of hand preferences). Hence, it can be hypothesized that larger-brained primates should evolve greater manual lateralization strength to reduce the amount of interhemispheric communication needed to accomplish manipulative tasks.

Given all this, testable hypotheses on primate hand preference evolution have long been established, but none of them have so far been assessed within quantitative evolutionary frameworks (Hopkins, 2013b). Studies on comparative cognition increasingly rely on phylogenetically informed modelling to estimate how and when specific behaviors evolved (MacLean et al., 2012; ManyPrimates et al., 2019 ; Krasheninnikova et al., 2020). Such approaches can provide estimates of ancestral states and allow researchers to quantify the influence of phylogeny and ecological variables on cognitive evolution (MacLean et al., 2012). However, to yield meaningful results, dense taxonomic sampling of species and a consistent testing scheme are required (Freckleton et al., 2002; Krasheninnikova et al., 2020). For research on primate hand preferences, this means that subjects from different species need to engage in the same experimental task to assess lateralization. Standardization is particularly important since both the strength and the direction of individual hand preferences can be task-dependent and because the expression of manual lateralization often correlates positively with motor complexity (Vauclair et al., 2005; Blois-Heulin et al., 2007; Lilak and Phillips, 2008; Meguerditchian et al., 2015; Caspar et al., 2018). Bimanual actions that involve both hands and which spontaneously occur during food manipulation or tool use are particularly suitable to detect hand preferences (Meguerditchian et al., 2013), while non-gestural unimanual actions such as grasping often do not elicit pronounced group- or individual-level lateralized responses (Papademetriou et al., 2005; Rogers, 2009; Hopkins et al., 2013b). However, habitual tool use is found in only a few lineages of primates (Musgrave and Sanz, 2018) and thus is only of limited use for comparative approaches. Therefore, bimanual actions related to foraging present themselves as suitable candidates for comparative studies on hand preferences in these animals.

A simple and widely applicable experiment to determine anthropoid primate hand preferences is the so-called tube task (Hopkins, 1995): A subject is handed a PVC tube filled with desired food. To extract it, one hand must hold the tube while the other has to engage in the more complicated action of retrieving the food mesh, thereby revealing biases in hand use dominance. Results from the tube task have been demonstrated to robustly correlate with hemispheric asymmetries in various primate groups (New World monkeys: Phillips and Sherwood, 2005; Old World monkeys: Margiotoudi et al., 2019; apes: Hopkins and Cantalupo, 2004; Dadda et al., 2006) and to be intraindividually consistent across re-tests, even if these were separated by several years (Hopkins et al., 2001). Furthermore, its simplicity allows uniform testing of a wide range of species in captive as well as natural settings (Zhao et al., 2012).

Here, we compiled a comprehensive multispecies tube task dataset to test pertaining hypotheses on the evolution of primate manual lateralization by means of phylogenetically informed modelling. This way we provide a broad comparative perspective on the origins of human right-handedness in the context of object manipulation.

Lateralization strength (MeanAbsHI) but not direction (MeanHI) displays a strong phylogenetic signal among anthropoids (Figure 1). Accordingly, MeanAbsHI (λ=0.89, p_{likelihood-ratio test} = 0.03) varied substantially between lineages but was often stable within groups of closely related taxa. MeanHI on the other hand showed random fluctuations around zero (λ<0.001; p_{likelihood-ratio test} = 1), and notable population level shifts toward either right- or left-hand preferences were uncommon (see below). Species-level distributions of hand preferences are summarized in Table 1 and are visualized at genus level in Figure 2.

Figure 1

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Figure 2

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Ancestral hand preference strength was modelled to have been similarly moderate in the stem lineages of hominoids (AbsHI = 0.606) and cercopithecoids (AbsHI = 0.627), while it was inferred to be higher in the ancestral platyrrhines (AbsHI = 0.740; Figure 1, Supplementary file 1). We found hand preference strength to be particularly weak among some species in the Papionina clade (baboons and their relatives) and to be least expressed in the gelada (Theropithecus gelada – MeanAbsHI = 0.257). The strongest preferences were found in humans (MeanAbsHI = 0.943), langurs of the genus Trachypithecus (MeanAbsHI = 0.868), and spider monkeys (Ateles spp. – MeanAbsHI = 0.831). Very pronounced individual preferences were also found in white-faced sakis (Pithecia pithecia – MeanAbsHI = 0.934) but our sample size for this species was notably small (n=7). In consequence, all aforementioned taxa included only very few, if any, ambipreferent individuals. Besides the saki genus Pithecia, the South Asian colobines Rhinopithecus and Trachypithecus were the only genera in which no ambipreferent individuals were found. Direction of manual lateralization was far more uniform across the anthropoid radiation than strength (Figure 1; Supplementary file 1). No species approached the extreme direction bias of humans (compare Figure 2), and only 2 of 37 non-human species exhibited a significant population-level bias as indicated by the one-sample t-test after correcting for multiple testing (4 of 37 when no correction was applied), namely gorillas and chimpanzees. Thus, such biases were restricted to the African ape lineage. After correcting for multiple testing, intraspecific frequencies of ambipreferent individuals, right-, and left-handers, as indicated by the chi-square goodness-of-fit test, differed significantly from the superordinate taxon estimate in four non-human species. These were chimpanzees, which are right-handed at the population level, and the predominately left-handed golden snub-nosed monkeys (Rhinopithecus roxellana), as well as geladas and black lion tamarins (Leontopithecus chrysopygus), both of which encompass a large proportion of ambipreferent individuals (Table 1). When omitting correction, respective biases were more frequent and found in 12 non-human species across the three major clades studied. Species- and genus-level results closely corresponded to each other (Table 1).

Our selected predictors for phylogenetic generalized least squares (PGLS) models showed a mixed and overall weak performance in explaining expression patterns of hand preference strength and direction in anthropoids (Table 2, Figure 3). For the initial model on lateralization direction, we found a significant effect of ecology, with terrestrial species displaying a right-hand bias compared to arboreal ones (p=0.04; Table 2A). However, when humans were removed from the model, this effect was merely recovered as a non-significant trend (p=0.07; Table 2B). Other predictors had no significant effect on lateralization direction, regardless of whether humans were considered in the model or not (p>0.2, Table 2A and B). When humans were included (Table 3A), models encompassing the component ecology as well as some considering brain size outperformed the lateralization direction null model. When humans were omitted from the analysis, the null model was solely outperformed by one that exclusively included the ecological component, and only slightly so (ΔAICc = 1.23; Table 3B), indicating a notable bias derived from the extreme right-handedness of our species. Thus, whereas habitual tool use and absolute brain size clearly do not influence the direction of lateralization among anthropoids in general, the analyses provide evidence for a weak but detectable effect of ecology in non-human taxa. Such ecological signatures were found to be of somewhat greater relevance for patterns of lateralization strength. Here, a significant negative effect of a terrestrial lifestyle was found (p=0.04; see Table 2C). In line with that, models including the component ecology consistently outperformed the null model, which was not the case for those including only tool use and/or brain size (Table 3C). Still, even the accuracy of the model relying on ecology alone exceeded that of the null model only moderately (ΔAICc = 2.53; Table 3C). Thus, terrestrial anthropoids tend to show weaker hand preferences than arboreal ones while there is no correlation with brain size or habitual tool use for this trait.

Figure 3

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At the individual level, Bayesian models showed that neither age nor sex had an influence on lateralization direction when the total sample was concerned (the respective credible intervals overlapped with zero; Supplementary file 2). However, we recovered a notable effect of age on lateralization direction in the hominoid subsample exclusively, with subadults tending more toward left-handedness than adults (credible interval = –0.28 to –0.01; Supplementary file 2). We observed a different pattern for lateralization strength. Here, an effect of age but again not sex was recovered for both the total sample (credible interval = –0.11 to –0.05) and the hominoid subsample (credible interval = –0.16 to –0.02), with weaker lateralization in subadults compared to adults. Such an influence of age was not detectable in neither platyrrhines nor cercopithecoids when these taxa were considered separately (credible intervals overlapping with zero; Supplementary file 2).

All data generated or analysed during this study have been deposited on Dryad: https://doi.org/10.5061/dryad.8sf7m0crv R code relevant to statistical analyses is deposited here: https://github.com/fpallasdies/CasparEtAl2022PrimateHandPreference.git, (copy archived at swh:1:rev:69cb316acaf82b1650386b5d8fcc9964e611ca01).

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Author details

1. Kai R Caspar

   1. Department of General Zoology, University of Duisburg-Essen, Essen, Germany
   2. Department of Game Management and Wildlife Biology, Faculty of Forestry and Wood Sciences, Czech University of Life Sciences, Praha, Czech Republic

   Contribution

   Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Visualization, Methodology, Writing – original draft, Project administration, Writing – review and editing

   For correspondence

   kai.caspar@uni-due.de

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-2112-1050

2. Fabian Pallasdies

   Institute for Theoretical Biology, Department of Biology, Humboldt-Universität zu Berlin, Berlin, Germany

   Contribution

   Data curation, Formal analysis, Investigation, Visualization, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-5359-4699

3. Larissa Mader

   Department of General Zoology, University of Duisburg-Essen, Essen, Germany

   Contribution

   Investigation, Writing – review and editing

   Competing interests

   No competing interests declared

4. Heitor Sartorelli

   Independent researcher, São Paulo, Brazil

   Contribution

   Investigation, Writing – review and editing

   Competing interests

   No competing interests declared

5. Sabine Begall

   Department of General Zoology, University of Duisburg-Essen, Essen, Germany

   Contribution

   Data curation, Formal analysis, Supervision, Investigation, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-9907-6387

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