Correction: Can Population-Level Laterality Stem from Social Pressures? Evidence from Cheek Kissing in Humans.

[This corrects the article DOI: 10.1371/journal.pone.0124477.].

Handedness for Unimanual Grasping in 564 Great Apes: The Effect on Grip Morphology and a Comparison with Hand Use for a Bimanual Coordinated Task.

A number of factors have been proposed to influence within and between species variation in handedness in non-human primates. In the initial study, we assessed the influence of grip morphology on hand use for simple reaching in a sample of 564 great apes including 49 orangutans Pongo pygmaeus, 66 gorillas Gorilla gorilla, 354 chimpanzees Pan troglodytes and 95 bonobos Pan paniscus. Overall, we found a significant right hand bias for reaching. We also found a significant effect of the grip morphology of hand use. Grasping with the thumb and index finger was more prevalent in the right compared to left hand in all four species. There was no significant sex effect on the patterns of handedness. In a subsample of apes, we also compared consistency in hand use for simple reaching with previously published data on a task that measures handedness for bimanual actions. We found that the ratio of subjects with consistent right compared to left hand use was more prevalent in bonobos, chimpanzees and gorillas but not orangutans. However, for all species, the proportion of subjects with inconsistent hand preferences between the tasks was relatively high suggesting some measures may be more sensitive in assessing handedness than others.

Can Population-Level Laterality Stem from Social Pressures? Evidence from Cheek Kissing in Humans.

Despite extensive research, the origins and functions of behavioural laterality remain largely unclear. One of the most striking unresolved issues is the fact that laterality generally occurs at the population-level. Why would the majority of the individuals of a population exhibit the same laterality, while individual-level laterality would yet provide the advantages in terms of improving behavioural efficiency? Are social pressures the key factor? Can social pressures induce alignment of laterality between the individuals of a population? Can the effect of social pressures overpass the effect of other possible determining factors (e.g. genes)? We tested this important new hypothesis in humans, for the first time. We asked whether population-level laterality could stem from social pressures. Namely, we assessed social pressures on laterality in an interactive social behaviour: kissing on the cheek as a greeting. We performed observations in 10 cities of France. The observations took place in spots where people of the city meet and greet each other. We showed that: a) there is a population-level laterality for cheek kissing, with the majority of individuals being aligned in each city, and b) there is a variation between populations, with a laterality that depends on the city. These results were confirmed by our complementary data from questionnaires and internet surveys. These findings show that social pressures are involved in determining laterality. They demonstrate that population-level laterality can stem from social pressures.

How should "ambidexterity" be estimated?

Weak and absent hand preferences have often been associated with developmental disorders or with cognitive functioning in the typical population. The results of different studies in this area, however, are not always coherent. One likely reason for discrepancies in findings is the diversity of cut-offs used to define ambidexterity and mixed right- and mixed left-handedness. Establishing and applying a common criterion would constitute an important step on the way to producing systematically comparable results. We thus decided to try to identify criteria for classifying individuals ambidextrous, mixed right- or left-handed or strong right- or left-handed. For that purpose, we first administered a handedness questionnaire to 716 individuals and performed multiple correspondence analyses to define handedness groups. Twenty-four participants were categorized as ambidextrous (3.3%), as opposed to mixed (29.2%) and strong (56%) right-handers, and to mixed (9.1%) and strong (2.4%) left-handers. We then compared this categorization with laterality index (LI)-based categories using different cut-offs and found that it was most correlated with LI cut-offs at -90, -30, +30 and +90, successively delimiting strong left-handedness, mixed left-handedness, ambidexterity (-30 to +30), mixed right-handedness and strong right-handedness. The characteristics of ambidextrous and lateralized individuals are also compared.

Hand preference and its flexibility according to the position of the object: a study in cercopithecines examining spontaneous behaviour and an experimental task (the Bishop QHP task).

The extant literature on manual laterality in non-human primates is inconclusive, plagued by inconsistent or contradictory findings and by disturbing methodological issues (e.g. uncontrolled influential factors, comparability issues). The present study examined hand preference and its flexibility in 15 red-capped mangabeys (C. t. torquatus) and 13 Campbell's monkeys (C. c. campbelli), two species that differ in their degree of arboreality. We investigated the influence of the spatial position of the object on hand preference for reaching. We considered spontaneous behaviour (reaching for food during daily feeding) and an experimental task: the QHP task. The QHP is a task that is used in humans. This is a simple reaching task that involves high spatial constraints on hand use. In our study, the subject had to reach for items that were placed on a semi-circle in front of it on five positions, including in the centre position, in the ipsilateral space and in the contralateral space. We assessed hand preference for reaching in front (baseline condition), and we examined how this preference changed when reaching in lateral positions. For reaching in front, about half of the subjects were lateralized and no group-level bias occurred, for both spontaneous and experimental conditions. When considering reaching in the lateral positions, we observed that the position of the object influenced hand use: individuals used the hand that was closest to the object. The results are discussed in relation to previous findings in humans and in non-human primates and regarding theories on handedness and flexibility of hand preference.

Lateralization for visual processes: eye preference in Campbell's monkeys (Cercopithecus c. campbelli).

Brain lateralization has been the matter of extensive research over the last centuries, but it remains an unsolved issue. While hand preferences have been extensively studied, very few studies have investigated laterality of eye use in non-human primates. We examined eye preference in 14 Campbell's monkeys (Cercopithecus c. campbelli). We assessed eye preference to look at a seed placed inside a tube using monocular vision. Eye use was recorded for 100 independent and non-rewarded trials per individual. All of the 14 monkeys showed very strong preferences in the choice of the eye used to look inside the tube (mean preference: 97.6%). Eight subjects preferred the right eye and six subjects preferred the left eye. The results are discussed in light of previous data on eye preference in primates, and compared to data on hand preference from these subjects. Our findings would support the hypothesis for an early emergence of lateralization for perceptual processes compared to manual motor functions.

Hand preferences for bimanual coordination in 29 bonobos (Pan paniscus).

Brain lateralization has long been thought to be unique to humans. To investigate the origins and functions of this feature, researchers study behavioural laterality in other animals. Despite a substantial database, manual laterality in non-human primates remains a controversial topic. We give here a review of the main findings on manual preference in great apes. This article presents data on hand preferences for a bimanual coordination in 29 bonobos (Pan paniscus). The study aims to provide data on manual laterality for a complex bimanual task in this very interesting and rarely studied species. Hand preferences were assessed using the 'tube task'. This task has been used with other species, which allows reliable data comparisons. The task requires a bimanual coordinated precise action: the subject holds the tube with one hand while reaching for food inside with the other hand. As a complex task, this measure has been shown to be efficient in revealing hand preferences. It has revealed group-level right bias in chimpanzees. Bonobos had never been tested. We recorded both independent bouts (counting only the first pattern of a sequence of identical actions) and frequency (counting every action). The bonobos exhibited strong hand preferences. With frequency, 11 bonobos were classified as right-handed, 15 were left-handed and 3 had no preference. With bouts, 8 bonobos were right-handed, 9 were left-handed and 12 had no preference. No group-level bias appeared. The results are discussed in relation with previous findings and theories on brain lateralization.

The evolution of handedness in humans and great apes: a review and current issues.

Population-level right-handedness is a defining characteristic of humans. Despite extensive research, we still do not know the conditions or timing of its emergence in human evolution. We present a review of research into the origins of handedness, based on fossil and archaeological data for hand preference and great ape hand-use. The data show that skeletal asymmetries in arm and hand bones supporting a rightsided dominance were present at least in the genus Homo, although data are more robust for Neanderthals. The evidence from tool-use, production, and cave art confirms that right-hand preference was established in Neanderthals and was maintained until the present. The great apes can provide real-life models for testing the conditions that facilitate or enhance hand preference at both the individual and group levels. The database on great ape hand-use indicates that they do exhibit hand preferences, especially in complex tasks. However, their preferences vary between tasks, and while group-level biases have occasionally been reported, no human-like handedness bias has been found. We discuss the methodological problems encountered in these approaches. Shared problems include a lack of agreed terminology both within and between disciplines, small sample sizes, interpretation biases and a failure to replicate experiments. In general, there is a paucity of fossil material, with poor preservation hampering traditional metric methods. The archaeological data are often founded on unreliable methods. The primate database is plagued by the use of measures that could be inappropriate for revealing hand preference, and by methodological inconsistencies between studies. We emphasise the need to standardise the methods to allow between studies and species comparisons. We propose that when referring to "handedness" it is more appropriate to use the terms "hand preference" and "hand use", to avoid confusion with each discipline's own definition of handedness.

Manual laterality in Campbell's Monkeys (Cercopithecus c. campbelli) in spontaneous and experimental actions.

Behavioural asymmetries, once thought to be exclusively human, appear to be widespread in vertebrates. A population-level bias should stem from natural selection and reflect a cerebral dominance, while individual preferences might be linked to individual characteristics. Manual laterality has been extensively investigated in non-human primates. However, despite a strong data base, no general patterns have emerged, resulting in a few explanatory theories and little consensus. This study was interested in manual laterality in 12 Campbell's monkeys (Cercopithecus c. campbelli). Several theories were examined, using both direct behavioural observations during feeding behaviour and six controlled experimental conditions, in which we varied task demands to investigate the effect of two factors. We systematically varied the individual posture (sat, tripedal, bipedal, clung) and the complexity of the task (box with or without a lid to open). Concerning the direction of preference, we found individual and action-specific preferences for experimental actions, which match previous reports. No population bias emerged and each subject appeared to react differently to the factors, hereby contradicting the theories. However, concerning the strength of preference, all individuals tended to be affected in similar ways. Spontaneous actions were less lateralized than experimental ones, and the simplest task and spontaneous category tended to show the weakest laterality. The relative complexity and novelty of these actions may account for these results.