Context-Dependent Gestural Laterality: A Multifactorial Analysis in Captive Red-Capped Mangabeys.

Catarrhine primates gesture preferentially with their right hands, which led to the hypothesis of a gestural origin of human left-hemispheric specialization for language. However, the factors influencing this gestural laterality remain understudied in non-hominoid species, particularly in intraspecific contexts, although it may bring valuable insights into the proximate and ultimate causes of language lateralization. We present here a preliminary investigation of intraspecific gestural laterality in catarrhine monkeys, red-capped mangabeys (Cercocebus torquatus). We described the spontaneous production of brachio-manual intentional gestures in twenty-five captive subjects. Although we did not evidence any significant gestural lateralization neither at the individual- nor population-level, we found that mangabeys preferentially use their right hands to gesture in negative social contexts, such as aggressions, suggesting an effect of emotional lateralization, and that they adapt to the position of their receiver by preferentially using their ipsilateral hand to communicate. These results corroborate previous findings from ape studies. By contrast, factors related to gesture form and socio-demographic characteristics of signaler and receiver did not affect gestural laterality. To understand better the relationships between gestural laterality and brain lateralization from an evolutionary perspective, we suggest that the gestural communication of other monkey species should be examined with a multifactorial approach.

Facial displays in red-capped mangabeys (Cercocebus torquatus): Repertoire, social context, and potential intentionality.

Primate communication relies strongly on the visual modality, notably through the production of a wide range of expressive facial signals. We investigated here the facial display repertoire of a relatively little-studied cercopithecid species, red-capped mangabeys (Cercocebus torquatus), and questioned whether their facial displays were dependent on social contexts and accompanied by indices of intentionality. Although the dual intentional and emotional use of apes' facial expressions has recently been suggested, the question of whether monkeys produce facial expressions intentionally to communicate remains open. We described 6 facial displays produced by captive red-capped mangabeys in social contexts. They are based on movements of the mouth, eyebrows, and ears, possibly graded in intensity and produced independently or in combination. We showed that most of the facial displays were produced preferentially in specific social contexts and that repertoires varied with subjects' characteristics, highlighting the communicative function of these displays. Moreover, behavioral markers of intentionality commonly used in gestural studies were found to accompany the production of some of the facial signals observed. Particularly, playful "open mouth" appeared strongly associated with intentionality indices, as previously noticed in ape species. All other facial displays, except yawns, did not exhibit all defined intentional indices but were, at least, directed toward a recipient. Interestingly, yawns presented different variants of intensity associated presumably with different social functions. Altogether, these results emphasize the communicative function of red-capped mangabeys' facial displays and provide a basis for further research on their intentional communication. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Red-capped mangabeys (Cercocebus torquatus) adapt their interspecific gestural communication to the recipient's behaviour.

Sensitivity to recipient's attention and responsiveness are critical markers of intentional communication. Although previous research showed that ape gestures can be intentional, few studies have yet addressed this question concerning monkeys. Here, we characterise the effect of a recipient's presence, attentional state and responsiveness on the interspecific gestural communication of captive red-capped mangabeys (Cercocebus torquatus). Previous reports showed that they produced learnt begging gestures towards a human recipient preferentially when the latter was facing them. We used here a novel setup that allows subjects to move around an experimenter and to use different modalities (visual and acoustic) to communicate. We found that when the recipient was not facing them, mangabeys moved to a position in the visual field of their recipient rather than using attention-getters. Interestingly, unlike apes, they did not elaborate their communication visually or acoustically when the experimenter did not respond favourably to their begging. However, our results may suggest that begging gestures were goal-directed, since mangabeys inhibited them when the experimenter was not available to answer immediately (i.e. give a reward). Overall, red-capped mangabeys' interspecific visual communication presented intentionality features, but their use of begging gestures was less flexible than that of great apes in similar situations.

The origins of gestures and language: history, current advances and proposed theories.

Investigating in depth the mechanisms underlying human and non-human primate intentional communication systems (involving gestures, vocalisations, facial expressions and eye behaviours) can shed light on the evolutionary roots of language. Reports on non-human primates, particularly great apes, suggest that gestural communication would have been a crucial prerequisite for the emergence of language, mainly based on the evidence of large communication repertoires and their associated multifaceted nature of intentionality that are key properties of language. Such research fuels important debates on the origins of gestures and language. We review here three non-mutually exclusive processes that can explain mainly great apes' gestural acquisition and development: phylogenetic ritualisation, ontogenetic ritualisation, and learning via social negotiation. We hypothesise the following scenario for the evolutionary origins of gestures: gestures would have appeared gradually through evolution via signal ritualisation following the principle of derived activities, with the key involvement of emotional expression and processing. The increasing level of complexity of socioecological lifestyles and associated daily manipulative activities might then have enabled the acquisition and development of different interactional strategies throughout the life cycle. Many studies support a multimodal origin of language. However, we stress that the origins of language are not only multimodal, but more broadly multicausal. We propose a multicausal theory of language origins which better explains current findings. It postulates that primates' communicative signalling is a complex trait continually shaped by a cost-benefit trade-off of signal production and processing of interactants in relation to four closely interlinked categories of evolutionary and life cycle factors: species, individual and context-related characteristics as well as behaviour and its characteristics. We conclude by suggesting directions for future research to improve our understanding of the evolutionary roots of gestures and language.

Human laterality for manipulation and gestural communication: A study of beach-volleyball players during the Olympic Games.

Comparative studies can help understand better brain functional lateralization for manipulation and language. This study investigated and compared, for the first time, human adults' laterality for manipulation and gestures in a non-experimental social context. We analysed the manual laterality of 48 beach volleyball athletes for four frequently expressed behaviours: a complex throwing action (jump serve) and three gestures (CLAP HAND, PUMP FIST and SLAP HAND-TO-HAND). We evaluated population-level laterality bias for each of the four behaviours separately, compared manual laterality between behaviours and investigated factors influencing gestural laterality. We furthered our between-gestures comparison by taking into account three categories of factors simultaneously: gesture characteristics (sensory modality), interactional context components (positions of interactants and emotional valence), and individual demographic characteristics (age, sex and country). Our study showed that (1) each behaviour considered presented a population-level right-hand bias, (2) differences of laterality between behaviours were probably related to gesture sensory modality and (3) signaller's laterality was modulated differently in relation to positions of interactants, emotional valence, age and sex. Our results support the literature suggesting that left-hemisphere specialization for manipulation and language (speech and gestures) may have evolved from complex manual activities such as throwing and from gestural communication.

Captive chimpanzees' manual laterality in tool use context: Influence of communication and of sociodemographic factors.

Understanding variations of apes' laterality between activities is a central issue when investigating the evolutionary origins of human hemispheric specialization of manual functions and language. We assessed laterality of 39 chimpanzees in a non-communication action similar to termite fishing that we compared with data on five frequent conspecific-directed gestures involving a tool previously exploited in the same subjects. We evaluated, first, population-level manual laterality for tool-use in non-communication actions; second, the influence of sociodemographic factors (age, sex, group, and hierarchy) on manual laterality in both non-communication actions and gestures. No significant right-hand bias at the population level was found for non-communication tool use, contrary to our previous findings for gestures involving a tool. A multifactorial analysis revealed that hierarchy and age particularly modulated manual laterality. Dominants and immatures were more right-handed when using a tool in gestures than in non-communication actions. On the contrary, subordinates, adolescents, young and mature adults as well as males were more right-handed when using a tool in non-communication actions than in gestures. Our findings support the hypothesis that some primate species may have a specific left-hemisphere processing gestures distinct from the cerebral system processing non-communication manual actions and to partly support the tool use hypothesis.

A multifactorial investigation of captive gorillas' intraspecific gestural laterality.

Multifactorial investigations of intraspecific laterality of primates' gestural communication aim to shed light on factors that underlie the evolutionary origins of human handedness and language. This study assesses gorillas' intraspecific gestural laterality considering the effect of various factors related to gestural characteristics, interactional context and sociodemographic characteristics of signaller and recipient. Our question was: which factors influence gorillas' gestural laterality? We studied laterality in three captive groups of gorillas (N = 35) focusing on their most frequent gesture types (N = 16). We show that signallers used predominantly their hand ipsilateral to the recipient for tactile and visual gestures, whatever the emotional context, gesture duration, recipient's sex or the kin relationship between both interactants, and whether or not a communication tool was used. Signallers' contralateral hand was not preferentially used in any situation. Signallers' right-hand use was more pronounced in negative contexts, in short gestures, when signallers were females and its use increased with age. Our findings showed that gorillas' gestural laterality could be influenced by different types of social pressures thus supporting the theory of the evolution of laterality at the population level. Our study also evidenced that some particular gesture categories are better markers than others of the left-hemisphere language specialization.

Human laterality for manipulation and gestural communication related to 60 everyday activities: Impact of multiple individual-related factors.

Literature on laterality emphasises the importance of implementing a comprehensive investigation of humans' and non-humans' laterality for both non-communication and communication functions. Adopting a global approach should enhance our understanding of the mechanistic drivers of human brain functional lateralisation and help to explore further the nature of the left-hemispheric systems for both functions. This study investigated human laterality for both functions by taking, for the first time, numerous behaviours and multiple potential influential factors into consideration. We analysed replies to the Rennes Laterality Questionnaire that takes into account simultaneously: participants' behavioural, demographic and social characteristics as well as their genetic/social learning components and collateral factors such as health problems. We collected and analysed a large data set including 450,220 item responses (317,594 items related to behavioural laterality and 132,626 items related to personal information) by 5904 participants. The majority of participants were right-lateralised for nine behavioural categories. The laterality of right-lateralised individuals for the behaviours considered varied very little between behavioural categories, contrary to the laterality of ambiguously- and left-lateralised individuals. This is the first evidence of the stability of right-lateralised individuals and the relative flexibility of ambiguously- and left-lateralised individuals with regards to behavioural laterality related to 60 everyday activities. Moreover, the laterality patterns of our study population were linked in particular to the following individual-related factors: demographic characteristics (current continent of residence), social characteristics (socio-professional group and study level), and collateral factors (writing hand, forced right-hand use, guiding eye, and health problems related to ear and back). We discuss our findings in relation to the evolutionary roots of human brain lateralisation for non-communication and communication functions.

Decision-making under risk of gain in young children and mangabey monkeys.

In contrast to human adults, risk proneness in the gain domain is usually observed in both young children and non-human primates. It is currently unclear what mechanism might be underlying such economic preferences. We investigated decision-making under risk of gain in toddlers and monkeys. The choices of 2.5-year-old children and red-capped mangabeys (Cercocebus torquatus torquatus) were examined in a gambling task for food reward in which participants have to choose between two options, a secure option and a risky option. In contrast to monkeys, toddlers showed a strong preference for the risky option over the safe option. In order to test the hypothesis that risky choices in participants reflect inhibitory control difficulties, toddlers and mangabeys were presented in Experiment 2 with a situation analogous to that used in Experiment 1 except for the fact that the opaque cover under which was placed the secure option was replaced by a transparent cover. In this second experiment, toddlers continued to show a preference for the risky option over the safe option. In contrast, mangabeys showed a preference for the safe option over the risky option in Trial 1 but they shifted their economic preferences in Trial 2. We argue that decision-making strategies under risk of gain in both toddlers and mangabeys (a) do not reflect poor behavioral control and (b) are not reducible to perception-action couplings.

Captive gorillas' manual laterality: The impact of gestures, manipulators and interaction specificity.

Relationships between humans' manual laterality in non-communicative and communicative functions are still poorly understood. Recently, studies showed that chimpanzees' manual laterality is influenced by functional, interactional and individual factors and their mutual intertwinement. However, what about manual laterality in species living in stable social groups? We tackled this question by studying three groups of captive gorillas (N=35) and analysed their most frequent manual signals: three manipulators and 16 gesture types. Our multifactorial investigation showed that conspecific-directed gestures were overall more right-lateralized than conspecific-directed manipulators. Furthermore, it revealed a difference between conspecific- and human-directed gestural laterality for signallers living in one of the study groups. Our results support the hypothesis that gestural laterality is a relevant marker of language left-brain specialisation. We suggest that components of communication and of manipulation (not only of an object but also of a conspecific) do not share the same lateralised cerebral system in some primate species.

Spontaneous approaches of divers by free-ranging orcas (Orcinus orca): age- and sex-differences in exploratory behaviours and visual laterality.

Running comparative studies of laterality in mammals is a way to deepen our understanding of the evolution of the brain hemisphere functions. Studies on vision highlighted a possible task-sharing between hemispheres depending on the characteristics of the observers, the nature of the observed stimulus and the context of the observation, a phenomenon that could go beyond the monitoring of conspecifics. Cetaceans are predators that adapted to an aquatic habitat and display a clear crossing of fibers to the side of the brain opposite the eye of origin. Here, we analysed the interactions between humans and cetaceans when free-ranging orcas approach divers. Our study concentrated on the spontaneous exploratory behaviours of divers by orcas depending on their age and sex, and on the possible expression of a visual laterality. The results showed a significant preference for the use of the left eye but exclusively in adult females. Adult males had a more sustained attention than adult females, marked by a higher spatial proximity to divers, slower approaches and longer look durations. Adult females, probably more cautious, explored from the distance and more furtively. Our findings support a possible link between attentional/motivational states and visual laterality in mammals.

Assessment and analysis of human laterality for manipulation and communication using the Rennes Laterality Questionnaire.

Despite significant scientific advances, the nature of the left-hemispheric systems involved in language (speech and gesture) and manual actions is still unclear. To date, investigations of human laterality focused mainly on non-communication functions. Although gestural laterality data have been published for infants and children, relatively little is known about laterality of human gestural communication. This study investigated human laterality in depth considering non-communication manipulation actions and various gesture types involving hands, feet, face and ears. We constructed an online laterality questionnaire including 60 items related to daily activities. We collected 317 594 item responses by 5904 randomly selected participants. The highest percentages of strong left-lateralized (6.76%) and strong right-lateralized participants (75.19%) were for manipulation actions. The highest percentages of mixed left-lateralized (12.30%) and ambidextrous (50.23%) participants were found for head-related gestures. The highest percentage of mixed right-lateralized participants (55.33%) was found for auditory gestures. Every behavioural category showed a significant population-level right-side bias. More precisely, participants were predominantly right-lateralized for non-communication manual actions, for visual iconic, visual symbolic, visual deictic (with and without speech), tactile and auditory manual gestures as well as for podial and head-related gestures. Our findings support previous studies reporting that humans have left-brain predominance for gestures and complex motor activities such as tool-use. Our study shows that the Rennes Laterality Questionnaire is a useful research instrument to assess and analyse human laterality for both manipulation and communication functions.

Intraspecific gestural laterality in chimpanzees and gorillas and the impact of social propensities.

A relevant approach to address the mechanisms underlying the emergence of the right-handedness/left-hemisphere language specialization of humans is to investigate both proximal and distal causes of language lateralization through the study of non-human primates' gestural laterality. We carried out the first systematic, quantitative comparison of within-subjects' and between-species' laterality by focusing on the laterality of intraspecific gestures of chimpanzees (Pan troglodytes) and gorillas (Gorilla gorilla) living in six different captive groups. We addressed the following two questions: (1) Do chimpanzees and gorillas exhibit stable direction of laterality when producing different types of gestures at the individual level? If yes, is it related to the strength of laterality? (2) Is there a species difference in gestural laterality at the population level? If yes, which factors could explain this difference? During 1356 observation hours, we recorded 42335 cases of dyadic gesture use in the six groups totalling 39 chimpanzees and 35 gorillas. Results showed that both species could exhibit either stability or flexibility in their direction of gestural laterality. These results suggest that both stability and flexibility may have differently modulated the strength of laterality depending on the species social structure and dynamics. Furthermore, a multifactorial analysis indicates that these particular social components may have specifically impacted gestural laterality through the influence of gesture sensory modality and the position of the recipient in the signaller's visual field during interaction. Our findings provide further support to the social theory of laterality origins proposing that social pressures may have shaped laterality through natural selection.

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.].

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.

Depressive-like behavioral profiles in captive-bred single- and socially-housed rhesus and cynomolgus macaques: a species comparison.

BACKGROUND: To unravel the causes of major depressive disorder (MDD), the third leading cause of disease burden around the world, ethological animal models have recently been proposed. Our previous studies highlighted a depressive-like profile among single- and socially-housed farm-bred cynomolgus macaques. Although phylogenetically close, cynomolgus and rhesus macaques, the two most commonly used macaque species in biomedical research, differ on several levels such as patterns of aggression, reconciliation, temperament, or dominance styles. The question of whether one captive macaque species was more vulnerable than another in the development of a pathological profile reminiscent of MDD symptoms was explored. METHODS: Behavioral data (including body postures, orientations, gaze directions, inter-individual distances, and locations in the cage) were collected in farming conditions. Using an unbiased validated ethological scan-sampling method, followed by multiple correspondence and hierarchical clustering analyses, 40 single- and 35 socially-housed rhesus macaques were assessed. Independently, for each housing condition, inter-species comparisons were made with previously acquired data on farm-bred cynomolgus monkeys. RESULTS: Consistent with our previous studies, we found depressive-like characteristics (e.g., inactivity, low level of investigation and maintenance, long time spent inactive while facing the wall) among single- and socially-housed rhesus macaques. Species-specificities were reported in non-depressive time budgets and in the prevalence of the pathological profiles. CONCLUSIONS: Our results suggest that rhesus may be more vulnerable to developing a despair-like state than cynomolgus macaques, both in single- and in social-housing conditions. Therefore, rhesus macaques are more suitable for use as a "spontaneous" model of depressive disorders.

Birth origin differentially affects depressive-like behaviours: are captive-born cynomolgus monkeys more vulnerable to depression than their wild-born counterparts?

BACKGROUND: Adverse early-life experience might lead to the expression of abnormal behaviours in animals and the predisposition to psychiatric disorder (e.g. major depressive disorder) in Humans. Common breeding processes employ weaning and housing conditions different from what happens in the wild. METHODS: The present study, therefore, investigated whether birth origin impacts the possible existence of spontaneous atypical/abnormal behaviours displayed by 40 captive-born and 40 wild-born socially-housed cynomolgus macaques in farming conditions using an unbiased ethological scan-sampling analysis followed by multifactorial correspondence and hierarchical clustering analyses. RESULTS: We identified 10 distinct profiles (groups A to J) that significantly differed on several behaviours, body postures, body orientations, distances between individuals and locations in the cage. Data suggest that 4 captive-born and 1 wild-born animals (groups G and J) present depressive-like symptoms, unnatural early life events thereby increasing the risk of developing pathological symptoms. General differences were also highlighted between the captive- and wild-born populations, implying the expression of differential coping mechanisms in response to the same captive environment. CONCLUSIONS: Birth origin thus impacts the development of atypical ethologically-defined behavioural profiles, reminiscent of certain depressive-like symptoms. The use of unbiased behavioural observations might allow the identification of animal models of human mental/behavioural disorders and their most appropriate control groups.

Baboons' hand preference resists to spatial factors for a communicative gesture but not for a simple manipulative action.

Olive baboons (Papio anubis) do acquire and use intentional requesting gestures in experimental contexts. Individual's hand preference for these gestures is consistent with that observed for typical communicative gestures, but not for manipulative actions. Here, we examine whether the strength of hand preference may also be a good marker of hemispheric specialization for communicative gestures, hence differing from the strength of hand preference for manipulative actions. We compared the consistency of individuals' hand preference with regard to the variation in space of either (i) a communicative partner or (ii) a food item to grasp using a controlled set-up. We report more consistent hand preference for communicative gestures than for grasping actions. Established hand preference in the midline was stronger for gesturing than for grasping and allowed to predict the consistency of hand preference across positions. We found no significant relation between the direction of hand preference and the task.

Social complexity parallels vocal complexity: a comparison of three non-human primate species.

Social factors play a key role in the structuring of vocal repertoires at the individual level, notably in non-human primates. Some authors suggested that, at the species level too, social life may have driven the evolution of communicative complexity, but this has rarely been empirically tested. Here, we use a comparative approach to address this issue. We investigated vocal variability, at both the call type and the repertoire levels, in three forest-dwelling species of Cercopithecinae presenting striking differences in their social systems, in terms of social organization as well as social structure. We collected female call recordings from twelve De Brazza's monkeys (Cercopithecus neglectus), six Campbell's monkeys (Cercopithecus campbelli) and seven red-capped mangabeys (Cercocebus torquatus) housed in similar conditions. First, we noted that the level of acoustic variability and individual distinctiveness found in several call types was related to their importance in social functioning. Contact calls, essential to intra-group cohesion, were the most individually distinctive regardless of the species, while threat calls were more structurally variable in mangabeys, the most "despotic" of our three species. Second, we found a parallel between the degree of complexity of the species' social structure and the size, diversity, and usage of its vocal repertoire. Mangabeys (most complex social structure) called twice as often as guenons and displayed the largest and most complex repertoire. De Brazza's monkeys (simplest social structure) displayed the smallest and simplest repertoire. Campbell's monkeys displayed an intermediate pattern. Providing evidence of higher levels of vocal variability in species presenting a more complex social system, our results are in line with the theory of a social-vocal coevolution of communicative abilities, opening new perspectives for comparative research on the evolution of communication systems in different animal taxa.