handedness and language

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Received: 26 January 2018    Revised: 23 October 2018    Accepted: 23 October 2018 DOI: 10.1111/eth.12827

PERSPECTIVES AND REVIEWS

History, development and current advances concerning the evolutionary roots of human right‐handedness and language: Brain lateralisation and manual laterality in non‐human primates Jacques Prieur

 | Alban Lemasson | Stéphanie Barbu | Catherine Blois‐Heulin

CNRS, EthoS (Ethologie animale et humaine) – UMR 6552, Universite de Rennes, Normandie Universite, Paimpont, France Correspondence Jacques Prieur, UMR 6552, Université de Rennes 1, Paimpont, France. Email: [email protected]

Abstract This review highlights the scientific advances concerning the origins of human right‐ handedness and language (speech and gestures). The comparative approach we adopted provides evidence that research on human and non‐human animals’ behav‐ ioural asymmetries helps understand the processes that lead to the strong human left‐hemisphere specialisation. We review four major non‐mutually exclusive envi‐

Funding information This study was conducted in the framework of a PhD funded by the French Ministry of Research and Technology with additional financial support of Rennes Metropole and the VAS Doctoral School.

human primates’ manual asymmetry: socioecological lifestyle, postural characteristics,

Editor: R. Bshary

mans’ manual laterality would have emerged from our ecological (terrestrial) and so‐

ronmental factors that are likely to have shaped the evolution of human and non‐ task‐level complexity and tool use. We hypothesise the following scenario for the evolutionary origins of human right‐handedness: the right‐direction of modern hu‐ cial (multilevel system) lifestyle; then, it would have been strengthened by the gradual adoption of the bipedal stance associated with bipedal locomotion, and the increas‐ ing level of complexity of our daily tasks including bimanual coordinated actions and tool use. Although hemispheric functional lateralisation has been shaped through evolution, reports indicate that many factors and their mutual intertwinement can modulate human and non‐human primates’ manual laterality throughout their life cycle: genetic and environmental factors, mainly individual sociodemographic char‐ acteristics (e.g., age, sex and rank), behavioural characteristics (e.g., gesture per se and gestural sensory modality) and context‐related characteristics (e.g., emotional context and position of target). These environmental (evolutionary and life cycle) fac‐ tors could also have influenced primates’ manual asymmetry indirectly through epi‐ genetic modifications. All these findings led us to propose the hypothesis of a multicausal origin of human right‐handedness. KEYWORDS

brain lateralisation, cerebral evolution, functional asymmetries, manipulation actions, multifactoriality

Ethology. 2019;125:1–28.

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1 |  I NTRO D U C TI O N 1.1 | State of the art concerning human right‐ handedness The asymmetrical structure of human brains for language‐related functions was first documented by Broca (1865). Since Broca’s pio‐ neering discovery, human cerebral laterality for motor, sensory, cog‐ nitive and emotional functions has been confirmed (e.g., Hugdahl & Davidson, 2002). Handedness is one of the most investigated fea‐ tures of laterality (e.g., Corballis, 2014; Llaurens, Raymond, & Faurie, 2009; Ocklenburg, Beste, & Güntürkün, 2013; Schmitz, Kumsta, Moser, Güntürkün, & Ocklenburg, 2017; Ströckens, Güntürkün, & Ocklenburg, 2013; Vallortigara & Versace, 2017; Willems, van der Haegen, Fisher, & Francks, 2014). Modern humans, at the population level, present a strong prefer‐ ence to use their right hand for manipulation activities, this meaning manual actions deprived of a communication function (e.g., Hecaen & de Ajuriaguerra, 1964; McManus, 1991; Prieur, Barbu, & Blois‐ Heulin, 2017). Ninety per cent of humans use their right hand pref‐ erentially for complex tasks such as writing, bimanual coordinated actions and tool use (e.g., Annett, 1985; Fagard, 2004; Faurie, 2004; Faurie & Raymond, 2004). Bimanual coordinated actions involve the use of both hands for different but complementary roles (i.e., manual role differentiation: Elliott & Connolly, 1984). For example, when manipulating an object, one hand holds the object while the other hand is engaged in a more active/complex action. We define tool use as the use of a detached object to modify the location or condition of another object or organism (Beck, 1980; Van Lawick‐ Goodall, 1970). Although humans are predominantly right‐handed for manipulation activities, reports evidenced geographical varia‐ tions of the proportions of right‐/left‐handed humans (e.g., Coren & Porac, 1977; Faurie, 2004; Faurie & Raymond, 2004; Marchant & McGrew, 1998; Marchant, McGrew, & Eibl‐Eibesfeldt, 1995; Perelle & Ehrman, 1994; Raymond & Pontier, 2004). For instance, the pro‐ portions of left‐handed individuals for writing ranged from 2.5% to 12.8% over 17 countries (Perelle & Ehrman, 1994). In addition, hu‐ mans’ right‐hand preference for communication activities has been evidenced. In the present review, the term “gesture” is restricted to communication functions and defined as “movements of the limbs or head and body directed towards a recipient that are goal‐directed, mechanically ineffective (i.e., they are not designed to act as direct physical agents) and receive a voluntary response” (Pika & Bugnyar, 2011; p 4). Reports concern undistinguished types of gestures ac‐ companying speech (e.g., Dalby, Gibson, Grossi, & Schneider, 1980, Kimura, 1973a, 1973b; Saucier & Elias, 2001), sign language by deaf adult speakers (e.g., Bellugi, 1991; Corina, Vaid, & Bellugi, 1992; Grossi, Semenza, Corazza, & Volterra, 1996; Vaid, Bellugi, & Poizner, 1989) and deictic gestures such as POINTING (from here, gestures are written in lower capitals) and/or symbolic gestures (e.g., to indi‐ cate “no” to someone) by toddlers, young children and human adults (e.g., Bates, O’Connell, Vaid, Sledge, & Oakes, 1986; Blake, 2000; Cochet & Vauclair, 2010a, 2010b, 2012, 2014 ; Vauclair & Imbault,

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2009; Young, Lock, & Service, 1985). Recently, Prieur et al. (2017 and Prieur, Barbu, and Blois‐Heulin (2018a) investigated human adults’ laterality for non‐communication and communication functions using the Rennes 1 Laterality Questionnaire, which includes 60 questions related to laterality in daily activities. The overwhelming majority of their 5,904 participants used predominantly their right‐body side not only for manipulation actions but also for the following eight catego‐ ries of gestures: iconic, symbolic, deictic (with and without speech), tactile, auditory, podial and head‐related gestures. Humans’ gestural communication involves brain regions similar to those processing spoken language (i.e., Broca and Wernicke’s areas) (e.g., Horwitz et al., 2003; Xu, Gannon, Emmorey, Smith, & Braun, 2009). Although 94%–96% right‐handed individuals for manipulation show a left‐brain hemisphere predominance for language, 4%–6% show a bilateral pat‐ tern (Pujol, Deaus, Losilla, & Capdevila, 1999; Springer et al., 1999). Conversely, 15%–30% left‐handed individuals for manipulation show atypical (bilateral or right‐hemispheric) language organisation (Josse & Tzourio‐Mazoyer, 2004; Knecht et al., 2000; Pujol et al., 1999). The ontogenetic and phylogenetic mechanisms leading to the overexpression of right‐hand use by humans are still diffi‐ cult to understand despite a substantial body of data. Reports provide evidence of a genetic basis of human handedness (e.g., Armour, Davison, & McManus, 2014; Corballis, 2014; McManus, Davison, & Armour, 2013; Ocklenburg, Beste, Arning, Peterburs, & Güntürkün, 2014; Somers, Shields, Boks, Kahn, & Sommer, 2015). For instance, studies showed the heritability of this trait as some families have a high rate of left‐handed individuals (e.g., Annett, 1973; Llaurens et al., 2009; McManus, 1991; Medland et al., 2010), and concordance of handedness is greater between monozygotic than dizygotic twins (e.g., McManus & Bryden, 1992; Sicotte, Woods, & Mazziotta, 1999). Adoption studies evidence that a child’s handedness is related more to that of its biological than its adoption parents (Carter‐Saltzman, 1980; Hicks & Kinsbourne, 1976; Saudino & McManus, 1998). Furthermore, handedness and neurodevelopmental disorders are genetically related (see also Brandler & Paracchini, 2014 for a review; e.g., Francks et al., 2007; Scerri et al., 2010). Scientific consensus is growing in favour of a multifactorial emergence of humans’ handedness that would be influenced by both genetic and epigenetic factors (e.g., Güntürkün & Ocklenburg, 2017; Ocklenburg et al., 2017; Ratnu, Emami, & Bredy, 2017; Schaafsma, Riedstra, Pfannkuche, Bouma, & Groothuis, 2009; Schmitz, et al., 2017; Schmitz, Metz, Güntürkün, & Ocklenburg, 2017; Sparrow et al., 2016). For instance, several studies investigated relationships between DNA methylation in buccal cells and handedness in healthy human adults to search for epigenetic biomarkers of handedness in non‐neuronal tissues (Leach, Prefontaine, Hurd, & Crespi, 2014; Ocklenburg et al., 2017; Schmitz, et al., 2017; Sun et al., 2005). These studies revealed that DNA methylation in various promoter regions can predict hand‐ edness direction. All these findings indicate that handedness is a complex trait continually shaped by a close intertwinement be‐ tween genetic and environmental (non‐genetic) factors.

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A number of reports provide evidence that environmental fac‐

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Corina, Jezzard, and Neville (2002) demonstrated that exposure

tors can modulate human handedness. Evidence for an environmen‐

to sign language (American Sign Language, ASL) leads to exten‐

tal basis of human lateralisation is founded on developmental factors

sive activation of the right‐hemisphere angular gyrus only in na‐

in prenatal and postnatal environments. Several studies suggested

tive signers (hearing, ASL‐English bilinguals) but not in those who

that lateralised behaviour is present during the early intrauterine

learned ASL after puberty (hearing, native English speakers). As

developmental stages. For instance, foetuses present a right‐side

Fagard (2013) concluded, the combination of genetic factors (po‐

bias when beginning to move one arm at 9–10 weeks of gestation

tentially influencing motor and postural asymmetries) as well as bi‐

(Hepper, Mccartney, & Shannon, 1998), sucking their thumb from

ological and cultural environmental factors occurring at different

14 to 15 weeks of gestation (Hepper, Shahidullah, & White, 1990,

periods during development could explain handedness. Cultural

1991), and turning their head in relation to their body from 14 weeks

environmental factors might also induce epigenetic modifications

of gestation (Hepper et al. 1990; Ververs, Vries, Geijn, & Hopkins,

affecting handedness indirectly (e.g., Güntürkün & Ocklenburg,

1994). Several reports showed a right‐side bias for adults’ head‐re‐

2017). In addition, gestures (e.g., signing and pointing), known to

lated gestures, suggesting that this head‐motor bias persists into

influence the development of language (Iverson & Goldin‐Meadow

adulthood (Barrett, Greenwood, & McCullagh, 2006; Chapelain

2005), could lead to a greater level of young children’s right‐hand‐

et al., 2015; Güntürkün, 2003; Karim et al., 2017; Ocklenburg &

edness than would non‐communication actions (Bates et al.,

Güntürkün, 2009; Prieur et al., 2017). The prevalence of turning

1986; Bonvillian, Richards, & Dooley, 1997; Cochet & Vauclair,

the head to the right during the last weeks of pregnancy would be

2010b; Cochet, Jover, & Vauclair, 2011; Esseily, Jacquet, & Fagard,

associated with the position of the foetus’s vertebral column with

2011; Jacquet, Esseily, Rider, & Fagard, 2012; Meunier, Vauclair,

respect to the mother (e.g., Fagard, 2013). Authors suggest that

& Fagard, 2012; Vauclair & Imbault, 2009). This could be related

this right‐side bias for the most frequent position (cephalic and to

to relatively independent developments of hand preference for

the left of the mother) could reinforce the right‐side motor system

communication and non‐communication functions (Jacquet et al.,

(e.g., Previc, 1991) and thus right‐handedness. Conversely, prenatal

2012). To our knowledge, as yet only Cochet and Vauclair (2012,

exposure to high levels of testosterone has been hypothesised to

2014 ) investigated this issue for human adults. They evidenced

play a role in the development of left‐handedness (e.g., Geschwind

greater right‐hand use for bimanual coordinated actions than for

& Galaburda 1985a, 1985b, 1985c). Male foetuses exposed to higher

POINTING produced without speech and an absence of significant

levels of prenatal testosterone than female foetuses present a slow‐

differences in the direction of laterality between bimanual coor‐

down in neuron growth in certain regions of their left cerebral hemi‐

dinated actions and POINTING produced with speech (Cochet &

sphere resulting in increased left‐hand use (Geschwind & Behan,

Vauclair, 2012). Furthermore, they reported no significant differ‐

1982; Geschwind & Galaburda, 1987). However, these findings must

ences in the direction of laterality between various types of ges‐

be considered with caution because other studies do not support

tures (declarative expressive POINTING, declarative informative

the Geschwind–Behan–Galaburda model of cerebral lateralisation

POINTING, imperative POINTING and symbolic gestures) and

in this area (e.g., Berenbaum & Denburg, 1995; Bryden, McManus,

non‐communication activities (Cochet & Vauclair, 2014). However,

& Bulman‐Fleming, 1994; Pfannkuche, Bouma, & Groothuis, 2009).

they showed stronger right‐hand use for declarative POINTING

Concerning the postnatal environment, longitudinal investigations of

than for non‐communication activities, whereas strength of lat‐

newborns evidenced a head position effect hypothesised to contrib‐

erality did not differ significantly between non‐communication

ute to the development of handedness (e.g., Michel, 1981; Konishi,

activities and imperative POINTING, or between non‐communi‐

Kuriyama, Mikawa, & Suzuki, 1987). Newborn infants who preferen‐

cation activities and symbolic gestures. To date, the results of the

tially directed their head towards the right at birth (Churchill, Igna,

approach of humans’ manual laterality by comparing communica‐

& Senf, 1962; Goodwin & Michel, 1981) and at 3–8 weeks (Michel,

tion and non‐communication functions are not well‐understood.

1981) were more likely to use later their right hand more than their

Recent genetic and functional neuroimaging (fMRI) studies em‐

left hand to reach and to grasp objects.

phasised the puzzling relationship between adults’ handedness

Evidence for an environmental basis of human lateralisation

and language (e.g., Badzakova‐Trajkov, Häberling, Roberts, &

is also based on cultural factors (e.g., see Llaurens et al., 2009;

Corballis, 2010; see also Bishop 2013; Güntürkün & Ocklenburg,

Schaafsma et al., 2009 for reviews). Social pressures can change

2017 for reviews; Häberling, Corballis, & Corballis, 2016; Knecht

the hand used for some activities such as forced right‐hand‐

et al., 2000; Liu, Stufflebeam, Sepulcre, Hedden, & Buckner,

edness for writing evidenced in several countries (e.g., France:

2009; Mazoyeret al., 2014; Ocklenburg et al., 2013; Ocklenburg

Dellatolas et al., 1988; Finland: Vuoksimaa, Koskenvuo, Rose, &

et al., 2014; Tzourio‐Mazoyer et al., 2015). For example,Häber‐

Kaprio, 2009; Germany: Siebner et al., 2002) and food‐related ac‐

ling et al., 2016) assessed asymmetric processing using fMRI for

tivities (e.g., Ivory Coast and Sudan: De Agostini, Khamis, Ahui,

three “gestural tasks” (observation of three sequences of actions:

& Dellatolas, 1997; Japan: Shimizu & Endo, 1983; Tunisia: Fagard

pantomimes, sign language and dog making movements) and two

& Dahmen, 2004). Likewise, social learning of sign language (that

“language tasks” (a word generation task and a synonym task).

implies extensive use of hand, arm and facial expressions) from

Their findings showed a left‐hemispheric bias for both language

birth could shape the structure of the brain. Newman, Bavelier,

and observation of gestures. The results of their factor analysis

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suggested three independent networks, a language‐linked net‐

Cerebral and behavioural asymmetry at the population level, once

work, a handedness‐linked network and a network representing

assumed to be unique to humans, has been documented for all ver‐

observations of manual actions independent of handedness. This

tebrate classes (i.e., fish: Sovrano, Rainoldi, Bisazza, & Vallortigara,

three‐way system would have evolved from manual actions, and

1999; amphibians: Robins, Lippolis, Bisazza, Vallortigara, & Rogers,

more specifically from primates’ mirror neuron system. Mirror

1998; reptiles: Deckel, 1995; birds: Vallortigara, 1992; and mam‐

neurons were first described in rhesus monkeys’ premotor cortex

mals: Casperd & Dunbard, 1996; see also Rogers, Vallortigara, &

(area F5) (e.g. review: Fabbri‐Destro & Rizzolatti, 2008). These

Andrew, 2013 for a review) and several phyla of invertebrates

particular visuomotor neurons discharge when a monkey performs

(insects: Letzkus et al., 2006; arachnids: Heuts & Lambrechts,

a given action and when it observes a similar action being per‐

1999; malacostracans: Takeuchi, Tobo, & Hori, 2008, gastropods:

formed by another individual (monkey or human). This area F5 is

Matsuo, Kawaguchi, Yamagishi, Amano, & Ito, 2010; cephalo‐

considered to be the homologue of the human Broca area respon‐

pods: Jozet‐Alves et al., 2012; and nematodes: Hobert, Johnston,

sible for language production.

& Chang, 2002; see also Frasnelli, 2013; Frasnelli, Vallortigara, & Rogers, 2012 for reviews). Cerebral and behavioural asymmetries

1.2 | Current issues

have been described for various functions including motor con‐ trol (e.g., limb laterality in birds: Brown & Magat, 2011; McGavin,

All these studies listed in the previous section indicate (a) the predomi‐

2009), sensory and cognitive functions (e.g., visual laterality in

nant involvement of humans’ left cerebral hemisphere in processing

cetaceans:Chanvallon, Blois‐Heulin, Latour, & Lemasson, 2017;

non‐communication actions and communication activities (speech and

Thieltges, Lemasson, Kuczaj, Böye, & Blois‐Heulin, 2011) and com‐

gestures); (b) the complex relationship between the directions of brain

munication (e.g., gestures in non‐human primates: Meguerditchian

lateralisation for manipulation and for language; and (c) that theoreti‐

& Vauclair, 2006; Hopkins et al., 2012; Prieur, Pika, Barbu, & Blois‐

cal multifactorial models (i.e., models considering multiple genetic and

Heulin, 2016a, 2016b). The apparent ubiquity of brain functional

non‐genetic influential factors) assuming several shared and unique

lateralisation in the animal kingdom would indicate that, in an

influential factors for handedness and for language would provide

evolutionary perspective, it would benefit biological fitness. The

the best fit with current empirical evidence to explain how handed‐

associated limb laterality has been massively reported among ver‐

ness and language lateralisation evolved and developed in individuals

tebrates. Nevertheless, although the body of research is still grow‐

(Ocklenburg et al., 2014). These results raise the following questions: Did our ancestors’ gestural communication contribute to the

ing, the phylogenetic mechanisms which lead to the overexpression of humans’ right‐hand use are still difficult to understand. Although

emergence of modern humans’ left‐hemisphere language specialisa‐

humans show a strong right‐hand preference at the population

tion? What is the nature of the left‐hemispheric systems involved in

level (e.g., McManus, 2002), non‐human animals’ limb preference

language (speech and gestures) and manipulation? In particular, are

varies with species. Ströckens et al., 2013) found that 61 of 119

manual behaviours performed in contexts involving manipulation and

animal species (51.3%) presented a population‐level limb bias, 20

gestural communication governed by distinct lateralised brain regions?

(16.8%), an individual‐level limb biases and 38 (31.9%) did not pre‐

From an evolutionary viewpoint, investigations of the be‐

sent any laterality bias.

havioural asymmetries of other animal species should help under‐

According to the evolution theory of laterality at the popula‐

stand better the processes that lead to the human left‐hemisphere

tion level (ELP) (Ghirlanda & Vallortigara, 2004; Ghirlanda,

specialisation for manipulation and gestural communication.

Frasnelli, & Vallortigara, 2009; Vallortigara, 2006; Vallortigara &

Based on a comparative approach, our review presents, first, a

Rogers, 2005), the development of cerebral lateralisation would

selection of studies highlighting the universal nature of lateral‐

have occurred in two steps. First, individual‐level biases would

ity in the animal kingdom; second, we focus on non‐human pri‐

have been selected because they provided cognitive advantages

mates’ manual laterality to extricate valuable clues. We discuss

for individual performance as, for example, saving neural space by

five main hypotheses concerning the evolutionary roots of human

avoiding replication of functions and hemispheric competition

right‐handedness and many factors modulating manual laterality

(e.g., Bisazza, De Santi, & Vallortigara, 1999; Corballis, 1989) and

throughout the life cycle. We end by integrating and synthesising

allowing simultaneous processing of different sources of informa‐

the literature for a better understanding of the evolutionary roots

tion (e.g., Rogers, 2002; Rogers, Zucca, & Vallortigara, 2004). For

of human right‐handedness.

instance, researchers comparing the performance of lateralised and non‐lateralised individuals showed that lateralisation im‐

2 |  B R A I N L ATE R A LI SATI O N : A W I D E S PR E A D PH E N O M E N O N

proves individual behavioural efficiency (e.g., spatial orientation of fish: Sovrano, Dadda, & Bisazza, 2005; foraging and monitoring predators by birds: Rogers, 2000, 2002 ; Rogers et al., 2004; hunting for cats: Fabre‐Thorpe, Fagot, Lorincz, Levesque, &

Many studies suggest that cerebral hemispheric laterality is older

Vauclair, 1993; foraging for non‐human primates: Butler, Stafford,

than previously thought (e.g., MacNeilage, Rogers, & Vallortigara,

& Ward, 1995; Fragaszy & Mitchell, 1990; Hopkins, Cantalupo,

2009; Vallortigara, 2006; Vallortigara, Rogers, & Bizazza, 1999).

Wesley, Hostetter, & Pilcher, 2002; Hopkins & Russell, 2004;

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McGrew & Marchant, 1992, 1999 ). Second, population‐level bi‐

other group members behind them. These findings are consistent

ases (i.e., unequal numbers of left‐ and right‐lateralised individu‐

with the ELP theory postulating that population‐level asymme‐

als in populations) could be the result of an evolutionarily stable

tries matter in social interactions and that social pressure may be

strategy (ESS)/frequency‐dependent selection based on inter‐

responsible for the alignment of laterality at the population level.

specific predator–prey interactions. This view is supported by a

This theory suggests that behavioural laterality at the population

game‐theoretical model (Ghirlanda & Vallortigara, 2004) suggest‐

level emerged in species subject to selection pressures imposed

ing that population‐level laterality biases in group living prey spe‐

by social interactions rather than in solitary species. This assump‐

cies subjected to predation would have produced advantages by

tion was first supported by empirical studies of visual laterality of

coordinating behaviours in the majority of the asymmetric indi‐

fish and tadpoles showing that population‐level laterality would

viduals of the population, but also disadvantages by making the

be more likely to be exhibited by social than by solitary species.

behaviour of individuals more easily predictable for negative in‐

These studies used various test apparatus where, for instance,

teractions such as predator–prey interactions (e.g., alignment of

subjects (a) faced their own mirror image; or (b) approached and

the direction of laterality by escaping shoaling fish: Bisazza,

inspected a dummy predator or a conspecific in a detour task

Cantalupo, Capocchiano, & Vallortigara, 2000; Vallortigara &

(fish: e.g., Bisazza et al., 2000; Cantalupo, Bisazza, & Vallortigara,

Bisazza, 2002). On the contrary, minority‐type individuals (e.g.,

1996; Sovrano et al., 1999; tadpoles: Bisazza, Santi, Bonso, &

human left‐handers) would be favoured in negative interactions

Sovrano, 2002; Dadda, Sovrano, & Bisazza, 2003). Intraspecific

such as fighting (e.g., strategic advantage of left‐handers in fenc‐

gestural laterality at the population level could also stem from

ing: e.g., Harris, 2010; see also Llaurens et al., 2009 for a review

social pressures as for the highly social non‐human great apes

concerning fitness costs and benefits acting as selective forces

(gorillas, chimpanzees) (Prieur, 2015; Prieur et al., 2016a; ; Prieur,

on the proportion of left‐handed people). More recently,

Barbu, Blois‐Heulin, & Pika, 2017; Prieur, Pika, Barbu, & Blois‐

Ghirlanda et al. (2009) game‐theoretical model study suggested

Heulin, 2017, 2018e ) and humans (Chapelain et al., 2015; Prieur

that population‐level laterality biases could be explained by an

et al., 2018a). For instance, Prieur and colleagues considering ges‐

ESS based solely on a trade‐off between antagonistic (competi‐

tures of chimpanzees’ and gorillas’ natural repertoire evidenced

tive) and synergistic (cooperative) intraspecific interactions.

effects of social pressures through the influence of social‐related

Whereas synergistic activities (e.g., cooperative hunting or effi‐

factors on their gestural laterality. Their laterality varied accord‐

cient use of the same tools) would favour individuals with the

ing to the following factors: group identity, signaller’s hierarchical

same lateralisation, antagonistic activities (direct competition

status, degree of dyadic affiliation (i.e., relationship quality) be‐

such as physical aggression or indirect such as competition for

tween signaller and recipient and/or sharing degree of gestures

resources) would favour minority‐type individuals. Therefore, so‐

within the population. Furthermore, by performing the first be‐

cial laterality (i.e., laterality expressed in social interactions) could

tween‐species statistical comparisons of intraspecific gestural

have arisen at the population level because it facilitated intraspe‐

laterality, the authors suggested that chimpanzees’ and gorillas’

cific interactions (Rogers, 2000). This assumption is supported by

social structure and dynamics could have impacted gestural later‐

studies in invertebrates (e.g., spitting spiders: Ades & Ramires,

ality differently through the influence of gesture sensory modal‐

2002; Heuts, Cornelissen, & Lambrechts, 2003; red wood ants:

ity and the position of the recipient in the signaller’s visual field

Frasnelli, Iakovlev, & Reznikova, 2012; fiddler crabs: Backwell et

during interactions (Prieur, Pika, Pika, Barbu, & Blois‐Heulin,

al., 2007) and vertebrates (e.g., fish: Bisazza et al., 1999; Bisazza

2017). Concerning gesture sensory modality, they found that go‐

et al., 2000; amphibians: Robins et al., 1998, Vallortigara, Rogers,

rilla signallers were more right‐handed than chimpanzee signal‐

Bisazza, Lippolis, & Robins, 1998; birds: Vallortigara, Cozzutti,

lers when performing auditory gestures. Auditory gestures

Tommasi, & Rogers, 2001; Ventolini et al., 2005; ungulates:

represent a greater part of gorillas’ (about one fifth) than of chim‐

Jennings, 2012; Versace, Morgante, Pulina, & Vallortigara, 2007;

panzees’ (about one‐tenth) gestural repertoires (Pika, Liebal, Call,

cetaceans: Karenina et al., 2010; Karenina, Giljov, Ivkovich,

& Tomasello, 2005). Prieur et al. hypothesised that this difference

Burdin, & Malashichev, 2013; primates: Baraud, Buytet, Bec, &

could be related to the fact that gorillas’ interindividual distances

Blois‐Heulin, 2009, Meguerditchian, Vauclair, & Hopkins, 2010;

(Klein, 1999) were generally greater than those of chimpanzees

Prieur et al., 2016a). For example, red wood ants exhibit a popu‐

(Harcourt, 1979), this would mean that auditory signals are partic‐

lation‐level bias during “feeding” contacts when a “donor” ant ex‐

ularly useful for gorillas to attract their social partners’ attention.

changes food with a “receiver” ant through trophallaxis: the

As the proportionof auditory gestures ingorillas’ repertoire is

“receiver” ant uses its right antenna predominantly more often

higherthan in chimpanzees’repertoire, these gestures might be

than its left antenna (Frasnelli, et al., 2012). Furthermore, Baraud

used more commonly and thus might be more codified/lateralised

et al. (2009) showed that social rank influenced mangabeys’ ap‐

in gorillas’ repertoire, resulting in potentially better social coordi‐

proach side as well as their relative transversal and vertical posi‐

nation. These findings concerning primates’ intraspecific gestural

tions: high‐ranking subjects were approached more frequently

laterality support the ELP theory (e.g., Ghirlanda & Vallortigara,

from their left than from their right. They showed that high‐rank‐

2004) as well as Ghirlanda et al. (2009) mathematical model pre‐

ing subjects were more likely than low‐ranking subjects to leave

dicting that population‐level biases could be explained by an ESS

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6      

based on intraspecific interactions. All these findings emphasise the importance of (a) studying laterality not only in interspecific interactions but also in intraspecific interactions; (b) considering

3.1 | Hypotheses concerning the evolutionary origins of human handedness

different behaviours and sensory modalities; and (c) taking into

Five main hypotheses aim to explain the origins of human manual

account multiple potential influential factors related to social in‐

asymmetry:

teractions in order to evidence effects of social pressures on laterality.

1. The postural origins hypothesis (MacNeilage, 2007; MacNeilage,

Despite all the scientific advances concerning laterality of limb

Studdert‐Kennedy, & Lindblom, 1987) stipulates that primate

use and laterality in social and non‐social behaviours, further studies

manual laterality would be the product of structural and func‐

are needed for a better understanding of the evolutionary origins of

tional adaptations for feeding. These adaptations would have

humans’ right‐handedness and left cerebral laterality for language

emerged in two steps. First, left‐hand preference would have

(speech and gestures) at the population level. With this aim in mind,

appeared for visually guided unimanual reaching to predate

the study of non‐human primates’ manual laterality, especially that

(e.g., fruit manipulation) while the right hand would have been

of great apes that are our closest relatives, should provide valuable

used to stabilise posture and arboreal locomotion. Second, the

clues (e.g., Corballis, 2002; Hopkins, 2007; MacNeilage, Studdert‐

evolution of primates towards terrestrial locomotion may have

Kennedy, & Lindblom, 1984; Meguerditchian, Vauclair, & Hopkins,

allowed them to be freed from postural restrictions associated

2013; Vauclair, Fagot, & Dépy, 1999).

with arboreal living conditions and consequently their right hand could become specialised for more demanding tasks such

3 |  N O N ‐ H U M A N PR I M ATE S ’ M A N UA L L ATE R A LIT Y FO R M A N I PU L ATI O N S A N D GESTURES

as bimanual manipulation. This hypothesis is supported by studies of arboreal species (orangutans: Hopkins et al., 2011; gibbons: Olson, Ellis, & Nadler, 1990; siamangs: Morino, 2011; Redmond & Lamperez, 2004; snub‐nosed monkeys: Zhao, Gao, & Li, 2010; De Brazza’s monkeys: Schweitzer, Bec, & Blois‐

Non‐human primates are widely used as research subjects be‐

Heulin, 2007; prosimians: Papademetriou, Sheu, & Michel, 2005)

cause they are the closest phylogenetic relatives to humans (e.g.,

as well as of more terrestrial species (gorillas, bonobos and

Langergraber et al., 2012; Sarich & Wilson, 1967; Scally et al., 2012).

chimpanzees:

Furthermore, they present striking similarities to humans concern‐

Meguerditchian, & Hopkins, 2005; rhesus macaques: Bennett,

Hopkins

et

al.,

2011;

baboons:

Vauclair,

ing hand anatomy (e.g., Aiello & Dean, 1990; Napier, 1962) and abil‐

Suomi, & Hopkins, 2008). On the contrary, this hypothesis is

ity to manipulate (e.g., Byrne, Corp, & Byrne, 2001; Napier, 1960)

not fully supported by other studies (e.g., reviews McGrew &

as well as neuroanatomical brain asymmetries for both hand motor

Marchant, 1997; Papademetriou et al., 2005) mainly of prosimian

functions and communication (e.g., Cantalupo & Hopkins, 2001;

behaviour. As far as we know, no reports evidence right‐hemi‐

Gannon, Holloway, Broadfield, & Braun, 1998; Hopkins & Pilcher,

sphere predominance (i.e., left‐hand preference) for prosimians’

2001; Hopkins, Russell, & Cantalupo, 2007, but see Wilson & Petkov,

visual spatial processing. This apparent contradiction would

2011 for evidence of bilateral sound communication processing by

suggest that lateralisation of primates’ hand function might

humans and macaques). Moreover, studies both in captivity and in

have emerged later than previously thought, maybe around

the wild have revealed the ability of some non‐human primates to

the time of the split between strepsirrhines and haplorhines

make and use tools (chimpanzees, e.g., Gruber, Clay, & Zuberbühler,

about 55 million years ago (Dodson, Stafford, Forsythe, Seltzer,

2010; McGrew & Marchant, 1992; bonobos, e.g., Kano, 1982;

& Ward, 1992; Falk & Byram, 2000; Scheumann, Joly‐Radko,

Roffman et al., 2015; gorillas, e.g., Grueter, Robbins, Ndagijimana,

Leliveld, & Zimmermann, 2011). The postural origins hypothesis

& Stoinski, 2013; Lonsdorf, Ross, Linick, Milstein, & Melber, 2009;

suggests a task‐complexity effect leading to right‐hand use

orangutans, e.g., Nakamichi, 2004; van Schaik, Fox, & Fechtman,

only for a certain level of demand and is in line with the four

2003; and capuchins, e.g., Lavallee, 1999; Visalberghi, 1990). Non‐

hypotheses mentioned below.

human primates are thus relevant models to explore the nature of

2. The bipedalism hypothesis also emphasises the link between pos‐

the relationships between human laterality and language as well as

ture and handedness as it postulates that postural/biomechanical

the origins of human right‐handedness and language (speech and

constraints associated with bipedal stance would be important

gestures).

factors underlying the emergence of group handedness (e.g., Falk,

To date, numerous studies and reviews have focused on non‐

1987; Sanford, Guin, & Ward, 1984; Westergaard, Kuhn, & Suomi,

human primates’ manual laterality (24th July 2017: Google Scholar

1998). According to this hypothesis, brain lateralisation would

indicated 12,000 research articles for “manual laterality in non‐

have provided motor skill advantages to adopt a bipedal posture,

human primates”). From this literature emerged several hypothe‐

which is naturally unstable and requires a complex control of a

ses on the evolutionary origins of human handedness, evidence of

moving body (e.g., to recover and to maintain balance stability fol‐

modulation of laterality by multiple factors and important meth‐

lowing a mechanical perturbation). In line with this hypothesis and

odological issues.

the appearance of human handedness, several non‐human

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      7

PRIEUR et al.

primate studies report a greater right‐hand use when in the bi‐

consequence of captivity and human presence. Differences in

pedal than in the tripedal posture (e.g., chimpanzees: Hopkins,

laterality patterns between results related to captive or wild en‐

1993; gorillas and orangutans: Olson et al., 1990) and a group‐

vironmental conditions could be influenced by methodological

level right‐hand bias for bipedal reaching (e.g., bonobos: Hopkins,

differences such as type of behaviour considered to evaluate

Bard, Bard, Jones, & Bales, 1993; chimpanzees: Hopkins, 1993:

hand preference (Hopkins, 1999; Hopkins & Cantalupo, 2004)

capuchins: Westergaard, Kuhn, Lundquist, & Suomi, 1997; see

and the nature of the task (e.g., Rogers, 2009). Indeed, as for the

also Westergaard et al., 1998 for a review). However, other non‐

following hypothesis considering task complexity, the existence

human primate studies report the opposite pattern, namely a left‐

and strength of manual laterality vary greatly with the nature of

hand preference for bipedal tasks (e.g., gorillas: Parnell, 2001;

the manipulation activity.

gibbons: Olson et al., 1990; lemurs: Forsythe & Ward, 1988).

4. The task‐complexity hypothesis proposed by Fagot and Vauclair

Although no consensus has been reached concerning the influ‐

(1991) predicts absence of laterality (an ambidextrous pattern) for

ence of bipedal posture on the direction of lateralisation, authors

tasks requiring a low level of manipulation (i.e., involving a single

agree that it influences the strength of lateralisation. Indeed, the

act such as reaching) but stronger hand preference for tasks im‐

vast majority of laterality studies indicate that bipedal posture in‐

plying a high level of manipulatory requirement (i.e., involving

creases primates’ (e.g., capuchins: Anderson, Degiorgio, Lamarque,

multiple acts such as bimanual coordinated actions and tasks im‐

& Fagot, 1996; galagos: Dodson et al., 1992) as well as marsupials’

plying complementary role differentiation). In accordance with

(e.g., eastern grey and red kangaroos: Giljov, Karenina, Ingram, &

this hypothesis, many studies show that complex bimanual behav‐

Malashichev, 2015) forelimb preference. Mammal laterality litera‐

iours elicit a significant right‐hand bias at the population level for

ture suggests that bipedalism played a major role in the evolution

chimpanzees (in the wild: Lonsdorf & Hopkins, 2005; in captivity:

of manual lateralisation and the appearance of humans’ robust

Hopkins, 1995; Hopkins et al., 2003; Hopkins et al., 2004; Hopkins

handedness.

et al., 2011; Llorente et al., 2011), gorillas (in the wild: Byrne &

3. The artefactual hypothesis argues that non‐human primates’ man‐

Byrne, 1991; in captivity: Hopkins et al., 2011; Meguerditchian,

ual laterality would be the product of experimental (Warren,

Calcutt, Lonsdorf, Ross, & Hopkins, 2010b), captive olive baboons

1980) and/or environmental factors related to captivity (McGrew

(Vauclair et al., 2005) as well as human infants (Potier,

& Marchant, 1997, 2001 ; Palmer, 2003). According to Warren

Meguerditchian, & Fagard, 2013) and adults (Cochet & Vauclair,

(1980), learning by induced practice (e.g., experimental device)

2012; Marchant et al., 1995). More generally, the expression of

would elicit stronger laterality than spontaneous daily actions

right‐handedness is positively correlated with increased complex‐

(e.g., simple reaching to pick up food off the floor). This assump‐

ity of manipulative activities:

tion is supported by studies of non‐human primates (e.g.,

a Between unimanual actions (e.g., simple reaching for food vs.

Chapelain, Bec, & Blois‐Heulin, 2006; Fagot & Vauclair, 1991;

wadge‐dipping by chimpanzees, Boesch, 1991; comparisons

Fragaszy & Adams‐Curtis, 1993; McGrew & Marchant, 1997;

between brachiating, and bipedal and tripedal standing to

Schweitzer et al., 2007; Trouillard & Blois‐Heulin, 2005).

reach food by red‐capped mangabeys, Blois‐Heulin, Guitton,

According to McGrew and Marchant (1997, 2001 ) and Palmer

Nedellec‐Bienvenue, Ropars, & Vallet, 2006; or to “grasp”

(2003), being raised by humans during infancy, artificial captivity

small vs. large food items by Tonkean macaques, Canteloup,

conditions and environmental stress could influence non‐human

Vauclair, & Meunier, 2013),

primates’ manual laterality; captive individuals would be more

b Between unimanual and bimanual coordinated actions (e.g., in

right‐handed than wild primates. In fact, some authors found an

the simple reaching for food task vs. in the coordinated bi‐

influence of human‐rearing on manual laterality for non‐commu‐

manual “tube task” for baboons, Vauclair et al., 2005; in the

nication actions (chimpanzees:Hopkins, 1994; Hopkins, et al.,

“box without lid task” that requires a simple unimanual action

1993; Hopkins, Bennett, Bales, Lee, & Ward, 1993) and gestures

vs. in the “box task” for Campbell’s monkeys, Chapelain et

(chimpanzees: Hopkins, 1999; Hopkins & Cantero, 2003).

al., 2006). The “tube task” is an experimental task first intro‐

However, growing evidence does not show a significant effect of

duced by Hopkins (1995) to study hand preference for biman‐

rearing history on laterality for non‐communication actions (e.g.,

ual coordinated actions: the subject has to extract food from

chimpanzees: Hopkins, 1995; Hopkins, Wesley, Izard, Hook, &

inside a tube with a finger while holding a baited tube with

Schapiro, 2004; Hopkins, Hook, Braccini, & Schapiro, 2003;

the other hand. The “box without lid task” is an experimental

Hopkins & Rabinowitz, 1997; Llorente et al., 2011; bonobos:

task introduced by Chapelain et al. (2006) to study hand pref‐

Chapelain, 2010), gestures (e.g., chimpanzees:Fletcher, 2006;

erence for unimanual actions: the subject has to take a seed

Hopkins & Leavens, 1998; Hopkins, et al., 2005; Hopkins, Russell,

out of an open box attached to the wire‐net inside its cage.

Cantalupo, Freeman, & Schapiro, 2005; Hopkins & Wesley, 2002)

The “box task” is an experimental task introduced by Forrester

or both non‐communication actions and gestures (pooled data)

and Quiatt (1994) to study hand preference for coordinated

(e.g., chimpanzees: Fletcher & Weghorst, 2005). Taking into con‐

bimanual actions: the subject has to take a seed out of a box

sideration these findings, we argue that population‐level hand‐

previously closed with a lid, the box being attached to the

edness in non‐human primates’ communication is not a

wire‐net inside its cage. The subject has to open the lid and

|

PRIEUR et al.

8      

keep it open with one hand while taking the seed with the

lifestyle (e.g., see Forrester et al., 2013; Steele, Ferrari, &

other hand.

Fogassi, 2012; Stout & Chaminade, 2012 for reviews).

Because of the positive correlation between the expression of right‐handedness and task complexity of manipulative activities, au‐

Thus, these five hypotheses suggest that ecological lifestyle (ar‐

thors proposed that laterality for complex tasks, particularly those

boreal and terrestrial), postural position (quadrupedal, tripedal and

requiring precise gripping as for tool use, would have served as a

bipedal stances), level of task complexity and tool use are four envi‐

pre‐adaptation for the emergence of left‐hemispheric lateralisation

ronmental factors likely to have influenced the evolution of human

for motor functions and human language (e.g., Bradshaw & Rogers,

and non‐human primates’ manual asymmetry. Recent between‐spe‐

1993; Breuer, Ndoundou‐Hockemba, & Fishlock, 2005; Forrester,

cies comparisons of intraspecific gestural laterality suggested that so‐

Quaresmini, Leavens, Mareschal, & Thomas, 2013; Frost, 1980;

cial lifestyle (social structure and dynamics) is an environmental factor

Gonzalez & Goodale, 2009; Greenfield, 1991; Hopkins, et al., 2007;

likely to have shaped primates’ manual asymmetry during evolution

Uomini, 2009). This has led several researchers to hypothesise that

(Prieur, et al., 2017). This comparative study of our close living relatives

tool use per se would have played a crucial role in the emergence of

(chimpanzees and gorillas) further supports the social theory of the or‐

human right‐handedness.

igins of laterality (e.g., see Ghirlanda & Vallortigara, 2004; Vallortigara

5. The tool use hypothesis postulates that the strong predominance

in determining the alignment of the direction of behavioural asymme‐

of right‐hand use by humans is a characteristic developed

tries at the population level through natural selection. Based on these

through tool use that was already present in humans’ and

findings, we hypothesised the following scenario for the evolutionary

great apes’ common ancestor (e.g., Breuer et al. 2005; Forrester

origins of human right‐handedness: modern humans’ right‐direction

& Rogers, 2005 for reviews) that postulates that social pressures acted

et al., 2013; Greenfield, 1991; Higuchi, Chaminade, Imamizu,

of manual laterality would have been shaped by our ecological (ter‐

& Kawato, 2009). This hypothesis is supported by studies

restrial) and social (multilevel system; e.g., Grueter, Chapais, & Zinner,

showing that right‐handed actions are associated with the ca‐

2012) lifestyle; then, it would have been strengthened by the gradual

pacity of the left cerebral hemisphere to deal with the complex

adoption of bipedal stance associated with bipedal locomotion, and

temporal sequences of motor activities required for tool making

the increasing level of complexity of our daily tasks including bimanual

and use (Foucart et al., 2005; Mercader et al., 2007; Weiss

coordinated actions and tool use. Furthermore, tool making and use

& Newport, 2006). Language capacity would thus have emerged

could have contributed to the evolution of human language. Although

as an extension of this left cerebral hemisphere capacity. This

functional lateralisation of the brain has been shaped through evolu‐

hypothesis is supported by brain imaging studies that evidence:

tion, researchers provided evidence that many intrinsic and extrinsic

first, homologues of left‐hemispheric anatomical specialisation

factors can modulate human and non‐human primates’ manual later‐

for language areas in great apes (e.g., Cantalupo & Hopkins,

ality through factors related to their life cycle such as individual so‐

2001; Gannon et al., 1998; Hopkins & Nir, 2010) known to

ciodemographic characteristics, context‐related characteristics and

make and use tools (e.g., chimpanzees: McGrew, 1992; bonobos:

behavioural characteristics (e.g., Meguerditchian et al., 2013; Prieur et

Kano 1982; gorillas: Grueter et al., 2013; orangutans: van Schaik

al., 2016a; Prieur et al., 2018a; J. Prieur, G. LeDu, M. Stomp, S. Barbu, &

et al. 2003); second, asymmetries in the homologues of human

C. Blois‐Heulin, unpublished data) These modulating factors concern‐

Broca’s and Wernicke’s areas associated with handedness for

ing non‐human primates are addressed below.

tool use in chimpanzees (Hopkins, et al., 2007); third, the overlap of brain activity for perceiving language and using tools in Broca’s area (Higuchi et al., 2009). These findings are con‐ sistent with studies showing neural correlates between language

3.2 | Factors modulating manual laterality through out the life cycle

and tool use, motorically complex manual actions and hierar‐

The literature indicates that many complementary intrinsic and ex‐

chical organisation of specific tool‐making methods (Faisal, Stout,

trinsic factors modulate the direction, strength and/or consistency

Apel, & Bradley, 2010; Johnson‐Frey, Newman‐Norlund, &

of manual laterality in both non‐communication actions and gestures

Grafton, 2004; Stout, 2011; Stout & Chaminade, 2007; Stout,

(within and across subjects and within and across tasks) of non‐human

Passingham, Frith, Apel, & Chaminade, 2011; Stout, Toth, Schick,

primate species including New World and Old World monkeys as well

& Chaminade, 2008; Uomini & Meyer, 2013). In addition, several

as Great apes (e.g., see McGrew & Marchant, 1997; Meguerditchian et

experiments evidenced the co‐evolution of hominine tool‐mak‐

al., 2013 for reviews). Four categories of factors must be considered

ing teaching and language (Lombao, Guardiola, & Mosquera,

when investigating the evolutionary roots of human right‐handed‐

2017; Morgan et al., 2015; Ohnuma, Aoki, & Akazawa, 1997;

ness: (a) individuals’ demographic characteristics (age, sex and group);

Putt, Woods, & Franciscus, 2014). Morgan et al. (2015) found

(b) individuals’ social characteristics (kinship, hierarchical and affili‐

that teaching and language, but not imitation or emulation,

ative relationships within groups); (c) context‐related characteristics

improve social transmission of stone tool manufacture. All these

(emotional context as well as the nature, position and characteristics

studies support specific co‐evolutionary relationships between

of target); and (d) behaviour per se and its characteristics.

laterality and tool use, language, gestures as well as social

Manual laterality increases with age

Age

No age effect on manual laterality

Results

Factor

Gestures

Non‐communication actions

Manipulatorsa

Gestures

Non‐communication actions

Behaviours

Meguerditchian and Vauclair (2006)

Olive baboon (Papio anubis)

Fagot, Drea, and Wallen (1991) Diamond and McGrew (1994)

Rhesus monkey (Macaca mulatta) Tamarins (Saguinus oedipus)

(Continues)

Fagot and Vauclair (1988), Meguerditchian and Vauclair (2009), Vauclair and Fagot (1987)

Olive baboon

Meguerditchian and Vauclair (2009)

Parr, Hopkins, and de Waal (1997)

Capuchin monkey

Olive baboon

Meguerditchian, Calcutt, et al. (2010)

Gorilla

Hopkins, et al. (2005)

Colell et al. (1995)

Bonobo

Chimpanzee

Hopkins (1993), Colell, Segarra, and Pi (1995)

Chimpanzee

Prieur, et al. (2017)

Prieur et al. (2018e)

Gorilla (Gorilla gorilla gorilla) Gorilla

Hobaiter and Byrne (2013), Hopkins and Leavens (1998), Prieur et al. (2018a)

Hook and Rogers (2000)

Marmoset (Callithrix jacchus) Chimpanzee

Ward, Milliken, Dodson, Stafford, and Wallace (1990)

Westergaard and Suomi (1993, 1994 )

Capuchinmonkey (Cebusapella)

Milliken, Stafford, Dodson, Pinger, and Ward (1991)

Rogers and Kaplan (1996)

Orangutan (Pongo pygmaeus pygmaeus)

Small‐eared bush baby (Otolemur garnettii)

Chapelain and Hogervorst (2009), Chapelain, Hogervorst, Mbonzo, and Hopkins (2011), Hopkins, et al. (1993), Hopkins, et al. (1993), Hopkins and de Waal (1995)

Bonobo (Pan paniscus)

Lemur (Lemur spp.)

Boesch (1991), Hopkins (1994, 1995 ), Humle and Matsuzawa (2009), Prieur et al. (2018b)

References

Chimpanzee (Pan troglodytes)

Species

TA B L E 1   Non‐exhaustive list of studies investigating the effects of age and sex on non‐human primates' manual laterality for communication and non‐communication functions

PRIEUR et al.       9

|

Meunier and Vauclair (2007), Phillips, Sherwood, and Lilak (2007), Spinozzi, Castorina, and Truppa (1998) Schweitzer et al. (2007) Laurence, Wallez, and Blois‐Heulin (2011) Meguerditchian, Donnot, Molesti, Francioly, and Vauclair (2012) Milliken et al. (1991)

Capuchin monkey De Brazza's monkey (Cercopithecus neglectus) Red‐capped mangabeys(Cercocebus torquatus) Squirrel monkey (Saimiri) Small‐eared bush baby

Meguerditchian and Vauclair (2006, 2009

Leliveld, Scheumann, and Zimmermann (2008)

Lemur (Microcebus murinus and M. lehilahytsara)

Olive baboon

Meguerditchian and Vauclair (2009)

Olive baboon

Hopkins, et al. (2005), Hopkins, et al. (2005), Meguerditchian, Vauclair, et al. (2010), Prieur et al. (2016a)

Meguerditchian, Calcutt, et al. (2010)

Chimpanzee

Hopkins (1995), Meguerditchian et al. (2015)

Gorilla

Hopkins and de Waal (1995)

Hopkins and Leavens (1998)

Chimpanzee

Bonobo

Chimpanzee

Prieur et al. (2018e)

Rogers and Kaplan (1996)

Orangutan

b

Sommer and Kahn (2009)

Human (Homo sapiens)

Gorilla

Byrne (2004), Corp and Byrne (2004), Hopkins, Russell, Schaeffer, Gardner, and Schapiro (2009)

References

Chimpanzee

Species

Manipulators are defined as mechanically effective social actions used to get things done (e.g., GRAB BODY). They imply physical/forceful handling of a recipient to attain the desired goal without direct and voluntary involvement of the recipient. bMale chimpanzees only showed a non‐significant trend (p