On the origins of human handedness and language: A comparative review of hand preferences for bimanual coordinated actions and gestural communication in nonhuman primates

Abstract

Within the evolutionary framework about the origin of human handedness and hemispheric specialization for language, the question of expression of population-level manual biases in nonhuman primates and their potential continuities with humans remains controversial. Nevertheless, there is a growing body of evidence showing consistent population-level handedness particularly for complex manual behaviors in both monkeys and apes. In the present article, within a large comparative approach among primates, we will review our contribution to the field and the handedness literature related to two particular sophisticated manual behaviors regarding their potential and specific implications for the origins of hemispheric specialization in humans: bimanual coordinated actions and gestural communication. Whereas bimanual coordinated actions seem to elicit predominance of left-handedness in arboreal primates and of right-handedness in terrestrial primates, all handedness studies that have investigated gestural communication in several primate species have reported stronger degree of population-level right-handedness compared to noncommunicative actions. Communicative gestures and bimanual actions seem to affect differently manual asymmetries in both human and nonhuman primates and to be related to different lateralized brain substrates. We will discuss (1) how the data of hand preferences for bimanual coordinated actions highlight the role of ecological factors in the evolution of handedness and provide additional support the postural origin theory of handedness proposed by MacNeilage [MacNeilage [2007]. Present status of the postural origins theory. In W. D. Hopkins (Ed.), The evolution of hemispheric specialization in primates (pp. 59-91). London: Elsevier/Academic Press] and (2) the hypothesis that the emergence of gestural communication might have affected lateralization in our ancestor and may constitute the precursors of the hemispheric specialization for language.

The Many Sides of Hemispheric Asymmetry: A Selective Review and Outlook

“…The other gestural network may be the residual of the original primate mirror system. This account lends some support to the view that language itself evolved from manual gestures rather than from vocal calls (Corballis, 2002;Hewes, 1973;Meguerditchian, Vauclair, & Hopkins, 2013), originating in the primate mirror system (Rizzolatti & Arbib, 1998).…”

Context-dependent lateralization of trunk movements in wild Asian elephants

“…Asian elephants, Elephas maximus, were examined both in captivity (Haakonsson and Semple, 2009) and in the wild (in Sri Lanka: Martin and Niemitz, 2003;in India: Keerthipriya et al, 2015), while a female African elephant, Loxodonta cyclotis, was observed in the zoo (Racine, 1980). In contrast to humans (Perelle & Ehrman 1994), great apes (Meguerditchian et al, 2013), bipedal marsupials (Giljov et al, 2015), parrots (Harris, 1989), anuran amphibians (Malashichev, 2006) and many other vertebrates (Ströckens et al,2013), elephants showed no population-level side biases in their manipulative behaviours neither with the use of the trunk nor with the use of the forelimbs (Haakonsson and Semple, 2009;Martin and Niemitz, 2003;Keerthipriya et al, 2015). However, taking into account that manifestation of motor lateralization depends on the nature of the task (Rogers, 2009), the full understanding of the lateralized trunk use in elephants cannot be gained without investigating it in different behavioural contexts.…”

“…This is in line with the general tendency observed in mammals. In primates, communicative motor actions, such as manual gestures, elicit more pronounced lateralization compared to non-communicative actions (Meguerditchian et al, 2013). Evidence for the absence of the population-level lateralization in non-social forelimb use has been reported in many nonprimate mammals, e.g., horses, Equus caballus (Austin and Rogers, 2012), dogs, Canis familiaris (Poyser et al, 2006, but see Wells, 2003 for subgroup biases in males and females), and bottlenose dolphins, Tursiops aduncus (Sakai et al, 2006).…”

Hand Preference during Tool Use in Wild Bearded Capuchins

“…Indeed, a considerable body of data shows that high-level motor tasks elicit a more robust, consistent and stronger degree of hand preference than low-level tasks (e.g. reaching) in various species of non-human primates particularly when using the tube task [Hopkins, 2013a;Meguerditchian et al, 2013]. De facto, population-level right-handedness has been reported in captive chimpanzees performing skilled manipulative activities [Hopkins et al, 2011] and neuroimaging data link asymmetries in the motor cortex with right-handed activities such as coordinated bimanual actions [Hopkins et al, 2007;Gilissen and Hopkins, 2013].…”