Research reportIntraspecific gestural laterality in chimpanzees and gorillas and the impact of social propensities
Introduction
Brain functional lateralization refers to the lateral specialization of functions between the left and right cerebral hemispheres of the brain. Studies investigating brain laterality have shown hemispheric specializations for various functions including laterality in vision (e.g. Quaresmini et al., 2014), facial expression (e.g. Wallez et al., 2012), and both manipulative and communicative functioning (e.g. see McGrew and Marchant, 1997, Meguerditchian et al., 2013 for reviews). For example, Meguerditchian and colleagues (2013) reviewed that humans and several species of non-human primate species exhibited a greater right-hand use in gestural communication than in non-communication actions. These findings thus indicate that gestures (from here, gestures are restricted to communication functions as defined by Pika and Bugnyar (2011)) and non-communication functions would be related to different lateralized cerebral substrates. However, despite substantial research efforts into the cerebral structures and functions in human and non-human species (e.g. Knecht et al., 2000, Hopkins et al., 2012, Ocklenburg and Güntürkün, 2012, Häberling and Corballis, 2016), mechanisms underlying brain functional lateralization are still unclear, even for human language related functions, although research devoted to language hemispheric specialization has received considerable attention since Broca’s pioneering discovery (Broca, 1865).
One of the reasons for this may be that the majority of human studies investigating language organization in the brain have naturally focused on verbal communication (spoken language). Moreover, although it is well established that the degree of language lateralization can vary across human subjects within a given verbal generation task (a commonly used activation task allowing the evaluation of expressive vocal communication: e.g. Knecht et al., 2000, Pirmoradi et al., 2016), only a few studies investigated how laterality can vary both within and between subjects across different verbal fluency tasks (e.g. Wilke et al., 2006, Wilke et al., 2010). In addition to this, there is virtually no research investigating language lateralization both within and between subjects across different gestural generation tasks (i.e. through a comparison between various types of distinct expressed gestures to study the stability of the direction of laterality at both the individual and population levels). Complementary studies are thus required 1) to extend and deepen knowledge of the multimodal character of human language with regards to brain lateralization by further investigating gestural communication, 2) to study hemispheric specialization at both the individual and population levels for different communication activities, and 3) to continue the exploration of the ontogenetic and phylogenetic mechanisms underpinning human brain lateralization for communication functions including gestural communication.
Research provided evidence that gestures play a crucial role in the communication of human and non-human primates (e.g. McNeill, 1992, Call and Tomasello, 2007, Pika, 2012). In particular, it has been shown that apes and monkeys’ gestural communication exhibit more intentionality and higher individual variability and flexibility than their vocal communication (e.g. Arbib et al., 2008, Meguerditchian and Vauclair, 2014). Although a growing number of authors supports the multimodal origins of language, many of them (e.g. Gentilucci and Corballis, 2006, Meguerditchian and Vauclair, 2014) postulate that gestural communication would be the phylogenetic precursor of human left-lateralized intentional communication system. According to these authors, this system would have then gradually included intentional vocalizations and oro-facial expressions to elaborate the multimodal nature of our language.
A relevant approach to better identify the proximate and distal causes of language lateralization is the evolutionary comparative approach that investigatesgestural laterality of humans’ closest phylogenetic relatives, the non-human primates. To apply this approach, it is especially important to take into account socio-ecological validity (i.e. to consider situations close to those where natural selection has and/or is still acting) and thus to favor the investigation of naturally occurring intraspecific gestural communication in non-human primates. To date, however, only a few studies have examined gestural laterality in non-human primates during spontaneously occurring communicative interactions between conspecifics. Among these studies, only those of Chapelain, 2010, Hobaiter and Byrne, 2013 and Prieur, 2015, Prieur et al., 2016 have examined the effect of potentially influential factors on purely intraspecific gestural laterality. For instance, by using a multifactorial approach, Prieur, 2015, Prieur et al., 2016 recently showed that chimpanzees’ intraspecific gestural laterality differed in relation to distinct gestural characteristics (e.g. sensory modality), interactional context components (e.g. emotional valence of the context), and individual socio-demographic characteristics of signaller and recipient (e.g. age, sex, and hierarchy). In addition, several studies have highlighted the possibility that ecological factors may influence manual laterality in non-communication actions (e.g. MacNeilage et al., 1987, Hopkins et al., 2011). However, to date no study has explored the higher-level ultimate causes (i.e. evolutionary forces) of the right-handedness/left-brain specialization for language considering purely non-human primates intraspecific gestures. In particular, the extent to which intraspecific gestural laterality has been shaped by the ecology and the sociobiology of a given species through natural selection needs to be addressed.
To contribute to this endeavour, the present study assessed and compared gestural laterality in spontaneously occurring communicative interactions between conspecifics in two great ape species, — chimpanzees (Pan troglodytes) and gorillas (Gorilla gorilla). Both species are phylogenetically very closely related to humans (e.g. Scally et al., 2012), live in relatively complex social groups (e.g. Goodall, 1968, Tutin, 1996) and show sophisticated gestural interactions (e.g. Call and Tomasello, 2007, Pika et al., 2003). Moreover, these two species differ in their ecology and their social structure and dynamics: chimpanzees are both terrestrial and arboreal (e.g. Doran, 1996) and live in multi-male–multi-female groups characterized by a highly variable party membership, whereas gorillas are mainly terrestrial (e.g. Ankel-Simons, 2007) and live in polygamous and generally cohesive groups (e.g. Aureli et al., 2008, Pika, 2007). Choosing such species with different ecology as well as social structure and dynamics will enable a better understanding of the possible influence of these socioecological factors on intraspecific gestural laterality.
To achieve this goal we studied three groups of chimpanzees and three groups of gorillas living in socio-ecologically relevant captivity conditions (i.e. when naturalization of enclosures is stimulating and social groups include many subjects). Such captivity conditions are ideal to study and compare non-human primates’ gestural communication because 1) they allow (unlike the wild) fairly physically comparable conditions in terms of opportunities for seeing one another, traveling, climbing, and so forth (e.g. Call and Tomasello, 2007), 2) growing evidence does not show a significant effect of captivity and human presence on laterality for non-communication actions (e.g. chimpanzees: Hopkins et al., 2003, Llorente et al., 2011) and gestures (e.g. chimpanzees: Hopkins et al., 2005, Fletcher, 2006), and 3) they enable to consider large sample size and number of data points per individual especially required to perform reliable and more comprehensive analysis (e.g. Prieur, 2015, Prieur et al., 2016).
We addressed the following two main research questions:
(Question 1) Do chimpanzees and gorillas exhibit stable direction of laterality when producing different types of intraspecific gestures at the individual level and is this related to the strength of laterality?
To answer this question, we investigated the production of the most frequent types of gestures produced by chimpanzees and gorillas which have been reported in well-established ethograms (Nishida et al., 2010) and gesture studies (chimpanzees: e.g. Call and Tomasello, 2007; gorillas: e.g. Pika et al., 2003). First, we separately assessed laterality at the individual level for 21 intraspecific gestures produced by chimpanzees and 16 produced by gorillas. Secondly, for both species we studied the possible relationships between the stability of the direction and strength of laterality in each gesture taken separately, then simultaneously considering all gestures. Based on literature showing an influence of gestural and individual sociodemographic characteristics on chimpanzees’ right-hand use (e.g. Hobaiter and Byrne, 2013, Prieur et al., 2016), we predicted firstly that we would find both ‘stable’ and ‘nonstable’ lateralized individuals. In other words, the direction of laterality in ‘stable’ individuals would not be dependent on the type of gesture per se whereas in ‘unstable’ individuals it would be gesture-specific (prediction n°1). Secondly, we expected that stable individuals would exhibit a higher degree of laterality than nonstable individuals (prediction n°2).
(Question 2) Is there a species difference in gestural laterality at the population level (i.e. when considering all our subjects as a whole)? If yes, which factors could explain this difference?
To answer this question, we examined the most frequent gestures shared by both chimpanzees and gorillas (a total of 14 shared gestures). We compared the direction and strength of gestural laterality between both species taking into account, first, each of these gestures (considered separately), then all gestures simultaneously (i.e. considered as a whole). Next, to further our between-species comparison, we performed a multifactorial investigation taking simultaneously into account the respective influences of the following three categories of factors previously found to modulate chimpanzees’ and gorillas’ gestural laterality (e.g. Prieur, 2015, Prieur et al., 2016): 1) interactional context components, 2) signal characteristics and 3) signaller’s socio-demographic characteristics. We predicted differences in gestural laterality between both species related to their socioecology and influenced by these three factors. More precisely, based on the postural origins theory of handedness for manipulation (MacNeilage et al., 1987, MacNeilage, 2007), we expected to find a difference in gestural laterality between both species related to their particular degree of arboreality/terrestriality (prediction n°3). As different species are known to show differences in laterality in relation to their different social structures (e.g. Sovrano et al., 1999, Bisazza et al., 2002), we predicted that gorillas living in relatively stable social groups (with gestural interactions with the same individuals possibly taking place at higher frequencies) would be more likely to exhibit stability in laterality (in direction and/or in strength) than chimpanzees which have less stable social structures including daily fission-fusion social dynamics and thus highly variable party memberships (prediction n°4).
Section snippets
Stability of the direction of chimpanzees’ and gorillas’ gestural laterality
To investigate whether and how chimpanzees and gorillas exhibit stable direction of gestural laterality at the individual level (Question 1), we first quantified their individual laterality bias focusing on the most frequently produced gestures of chimpanzees (N = 21) and gorillas (N = 16) reported in previous studies (e.g. Nishida et al., 2010, Pika et al., 2003). We then examined the potential relationships between stability of the direction and strength of gestural laterality. Over all the
Discussion
The aim of the present study was to contribute to the investigation of the proximate and distal causes of the right-handedness/left-brain specialization for language by considering the laterality of chimpanzees’ and gorillas’ most frequently expressed intraspecific gestures. To do so, we addressed two main research questions. Firstly, do chimpanzees and gorillas exhibit stable direction of laterality when producing different types of gestures at the individual level and if yes is it related to
Experimental procedures
A more detailed description of all subjects and of the observational and coding procedures can be found in previous studies (Prieur, 2015, Prieur et al., 2016).
Funding
This study has been performed 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. In addition, it was supported by a Sofja Kovalevskaja-Award of the Humboldt Foundation to S. P.
Acknowledgments
We are very grateful to all the keepers, collaborators and researchers of the Wolfgang Köhler Primate Research Center at Zoo Leipzig (Germany), the Zooparc de Beauval, the zoo of La Palmyre, the zoo of La Vallée des Singes (France), the zoo of Apenheul and the Burgers’ zoo (Netherlands). We are indebted to J. Call, A. Desmoulins, J.-P. Gury, D. Hanus, F. Perroux, T. Petit, R. Potier, F. Rietkerk, and W. Schoo for allowing us to study the chimpanzee and gorilla groups at the respective zoos and
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