Review Reports - Limb Preference in Animals: New Insights into the Evolution of Manual Laterality in Hominids

Round 1

Reviewer 1 Report

I found this to be an important review paper that can be of high interest to specialist readers. Authors conceptualize the current understanding of manual lateralization in primates and other animals. The most significant empirical evidence available at the moment is discussed. The study provides a review and a summary of the most recent findings together with the key ‘classic’ studies of the past. No doubt this is crucially important for further development of our understanding of this field. I really enjoyed reading because the depth of the analysis and the simplicity and clarity of the text is very well balanced throughout the manuscript.

My only minor concern is that not all relevant references were included (see my specific comments below).

L 90-96: The sentence is too long and too complex to be readily understandable. Please consider dividing it into at least two sentences.

L 179-184: There may be relevant to mention the studies of the ontogeny of manual preferences in non-primates species, e.g., Wells, D. L., & Millsopp, S. (2012). The ontogenesis of lateralized behavior in the domestic cat, Felis silvestris catus. Journal of Comparative Psychology, 126(1), 23. In addition, a very early expression of lateralized motor behavior is a characteristic of handedness that is consistent between humans and bipedal marsupials. In a macropod, the species-typical pattern of lateralized forelimb use was found to be evident already at a pouch young stage.

L 317: Two different phenomena are mixed together here. There is a postural effect on an individual (i.e. the increased manual preference in an individual in the upright posture as compared to quadrupedal posture) and on a species (i.e. stronger lateralization in more bipedal species as compared to quadrupedal species). The postural effect on an individual has been found e.g., in humans and non-human primates (e.g., Westergaard GC, Kuhn HE, Suomi SJ (1998) Bipedal posture and hand preference in humans and other primates. J Comp Psychol 112: 56–63.). Limb preferences in a marsupial, Macropus rufogriseus: evidence for postural effect. Animal Behaviour, 83(2), 525-534.). Studies on cats and tree shrews mentioned in the manuscript both tested this effect and failed to find it in these species. The postural effect at the interspecies level has been traced in primates (e.g., Ward JP (1995) Laterality in African and Malagasy prosimians. In: Alterman L, Doyle GA, Izard MK. Creatures of the Dark: the Nocturnal Prosimians. New York: Plenum. pp. 293–309） Laterality in quadrupedal and bipedal prosimians: reach and whole-body turn in the mouse lemur (Microcebus murinus) and marsupials (ref. in the MS).

L 336-340: It has been proposed that cultural differences in the manifestation of human handedness could be associated not only with cultural difference but also with the types of manual activity studied. It has been found that the degree of right-hand preference in manual activity not associated with tool use is generally relatively weak. A study of three traditional pre-literate human societies had shown weak overall right-hand bias for non-tool-use behaviours. This has led the authors to a plausible conclusion, suggesting that the traditional testing paradigms that focus on precision tool use give ‘an artefactual, biased picture of extreme lateralisation’ [6, p. 256]. I believe this is worth mentioning somewhere in your review.

L 478-479: Moreover, Left-cradling bias is evident in adults even when they only imagine holding an infant, but actually are holding an inanimate object (ref. 185).

L 530: I believe that lateralized embraces in primates are worth mentioning in the section of the paper devoted to the social effect on manual biases: Boeving, E. R., Belnap, S. C., & Nelson, E. L. (2017). Embraces are lateralized in spider monkeys (Ateles fusciceps rufiventris). American Journal of primatology, 79(6), e22654.

Author Response

Reviewer 1:

→ We thank the reviewer for this very positive feedback on our manuscript. Please find below our detailed response to specific comments.

L.90-96: The sentence is too long and too complex to be readily understandable. Please consider dividing it into at least two sentences.

→ Thank you for this suggestion: we have divided this statement into two sentences (L.91-97):

“ Comparative research done in the past years has been a real opportunity to better understand the different functions in which limb use is lateralized, and thus better assess the adaptive explanations for the evolution of limb lateralization by better understanding the different selective pressures that may have driven this evolution. Recent studies have further considered that - besides adaptive explanations - the acquisition of handedness may be related to variations in developmental trajectories in other traits across ontogeny. “

L.179-184: There may be relevant to mention the studies of the ontogeny of manual preferences in non-primates species, e.g., Wells, D. L., & Millsopp, S. (2012). The ontogenesis of lateralized behavior in the domestic cat, Felis silvestris catus. Journal of Comparative Psychology, 126(1), 23. In addition, a very early expression of lateralized motor behavior is a characteristic of handedness that is consistent between humans and bipedal marsupials. In a macropod, the species-typical pattern of lateralized forelimb use was found to be evident already at a pouch young stage.

→ Thank you very much for this suggestion! We have added the following paragraph (L. 193-207) including the elements brought out in those two studies:

“Regarding the ontogeny of limb preferences in non-primate species, Wells & Millsopp [63] ( investigated the development of paw preferences in the domestic cat (Felis silvestris catus) and reported a significant effect of age: while individuals were more ambilateral at 12 weeks of age than at later developmental stages, paw preferences at 6 months and at 1 year of age were positively correlated. In marsupial species, the red-necked wallaby (Macropus rufogriseus) and the eastern gray kangaroo (Macropus giganteus) show a left-forelimb preference (for manipulating food) at population-level as soon as the pouch young stage (approximately 6–7 and 7–9 months old, respectively) [64]. In the eastern gray kangaroo, the authors compared limb-preferences in manipulative behavior at different developmental stages, namely before and shortly after individuals display the bipedal posture (young-at-foot, approximately 11–15 months old): as they observed no difference between these two juvenile stages and the adult stage, the authors concluded that « manual lateralization in bipedal marsupials is not determined by the acquisition of habitual bipedality » but precedes it in the course of ontogenesis [64] (p.1).

L.317: Two different phenomena are mixed together here. There is a postural effect on an individual (i.e. the increased manual preference in an individual in the upright posture as compared to quadrupedal posture) and on a species (i.e. stronger lateralization in more bipedal species as compared to quadrupedal species). The postural effect on an individual has been found e.g., in humans and non-human primates (e.g., Westergaard GC, Kuhn HE, Suomi SJ (1998) Bipedal posture and hand preference in humans and other primates. J Comp Psychol 112: 56–63.). Limb preferences in a marsupial, Macropus rufogriseus: evidence for postural effect. Animal Behaviour, 83(2), 525-534.). Studies on cats and tree shrews mentioned in the manuscript both tested this effect and failed to find it in these species. The postural effect at the interspecies level has been traced in primates (e.g., Ward JP (1995) Laterality in African and Malagasy prosimians. In: Alterman L, Doyle GA, Izard MK. Creatures of the Dark: the Nocturnal Prosimians. New York: Plenum. pp. 293–309） Laterality in quadrupedal and bipedal prosimians: reach and whole-body turn in the mouse lemur (Microcebus murinus) and marsupials (ref. in the MS).

→ We are thankful for this very helpful comment. We made modifications on this paragraph so that postural effect at the interspecies level is first explained (i.e. effect of species’ locomotory styles on laterality as evidenced by comparative studies).

We then cited works on postural effect on individuals (i.e. effect of bipedal / quadrupedal posture at the moment of the task performance) as an illustration of the constraints exerted by postural support on manual laterality (L.379-389):

“In addition to the above-cited observations suggesting that species locomotory style affects manual laterality, the PO theory is supported by findings on postural effects at the individual level in several mammal species. Indeed, an increased manual preference can be observed human and non-human primates performing manual tasks in a bipedal compared to quadrupedal posture [60,115–118]. Similar observations has been made in other mammals, such as red-necked wallabies (Macropus rufogriseus) [115] (but see absence of postural effect in tree shrews, Tupaia belangeri [119]; and in cats, Felis silvestris catus [120]). This corroborates the hypothesis that the need for postural support acts as a constraint on hand availability for manual actions, and so on manual laterality. The PO theory proposes this as a critical evolutionary mechanism which would have shaped handedness emergence.”

L.336-340: It has been proposed that cultural differences in the manifestation of human handedness could be associated not only with cultural difference but also with the types of manual activity studied. It has been found that the degree of right-hand preference in manual activity not associated with tool use is generally relatively weak. A study of three traditional pre-literate human societies had shown weak overall right-hand bias for non-tool-use behaviours. This has led the authors to a plausible conclusion, suggesting that the traditional testing paradigms that focus on precision tool use give ‘an artefactual, biased picture of extreme lateralisation’ [6, p. 256]. I believe this is worth mentioning somewhere in your review.

→ We thank the reviewer for this really interesting suggestion. We cited the corresponding study in the last part of the paper, in which we discuss task complexity effect on manual lateralisation and resulting bias in inter-study comparisons focusing on different tasks.

L.1040-1050:“Marchant et al. [366] described humans’ manual preferences in diverse spontaneous actions, based on film archives of three traditional societies. They evidenced only a weak overall lateralization for manual actions (barely above 50% of right-hand use in the three study populations), but interestingly found a greater right-hand preference when specifically considering precision tool use (above 84% of right-hand use). The authors thus noted that “the disparity between the ethological and the typical psychological findings on handedness may thus be simply explained: questionnaire and performance testing paradigms focus only on a small and selected proportion of manual activities, those to do with tool use, and especially with skilled, fine-motor tool use. This gives an artefactual, biased picture of extreme lateralization.” (p. 256). “

L.1060-1062:“Moreover, assessing human handedness based on ethological descriptions of spontaneous manual activities may provide more reliable research material to compare with animal observations.”

L.478-479: Moreover, Left-cradling bias is evident in adults even when they only imagine holding an infant, but actually are holding an inanimate object (ref. 185).

→ Thank you for suggesting this relevant reference.

We added a description of this study (L.611-615):

"A study even asked adult humans (n=300, including both women and men) to imagine themselves holding in their arms an object (I.e., either an expensive vase or an old shoebox) and then an infant (i.e., about 3 months of age): while a right-cradling bias was reported for both imagined objects, a left-cradling bias (i.e., 66%) was reported for holding the imagined infant [194]."

L.530: I believe that lateralized embraces in primates are worth mentioning in the section of the paper devoted to the social effect on manual biases: Boeving, E. R., Belnap, S. C., & Nelson, E. L. (2017). Embraces are lateralized in spider monkeys (Ateles fusciceps rufiventris). American Journal of primatology, 79(6), e22654.

→ Thank you for notifying that this reference was missing:

We added a reference to this study to discuss the effect of social laterality on manual biases (L.939-945).

“as several primates favor one side or another to approach conspecifics, notably depending on dominance relationships (e.g. in red-capped and grey-cheeked mangabeys, Cercocebus torquatus and Lophocebus albigena [344]) or depending on the type of interactions (e.g., embracing and grooming in Colombian spider monkeys, Ateles fusci-ceps rufiventris [345], it may be hypothesized that social laterality affects manual preferences in social interactions, including for gestural communication.

Reviewer 2 Report

This is an excellent review of the evidence for hand preferences in primates and limb preferences in some other vertebrate species. Although I have suggested some addition literature that should be cited, the review is comprehensive and makes a valuable contribution to the field.

147: Something is missing inside the brackets.

165: Change ‘dependent from’ to ‘dependent on’.

204-207: The paper by Brown and Magat (2011) has been cited incorrectly. This paper shows that footedness may be associated with body size and diet in Australian parrots. It does not show that “brain lateralization in Australian parrots is highly correlated with “hand”(i.e. foot) preference..”. In fact, the Brown and Magat paper did not investigate brain lateralization per se. A more recent paper, not yet cited in this review, has shown that strength and direction of foot-preference in Australian parrots is correlated with brain size (Kaplan and Rogers, 2021, Brain size associated with foot preferences in Australian parrots. Symmetry 13, 867). This paper should be cited and discussed in this part of the text.

239: Change claws to claw.

248: Change take to taking.

385-420: In this section it would be well-worth discussing the association between hand preference and approach/withdrawal, as well as cognitive bias, shown in marmosets. See Rogers (2009) Phil. Trans. R. Soc. 364, 943-954.

450: Change ‘than in primates’ to ‘as in primates’.

462-470: I am not sure whether the evidence for left-laterality in fruit-flies is relevant here. Although it is interesting, left lateralization in insects may mean use of the left side of the brain since there is an absence of the mid-line crossing characteristic of vertebrates. It would be better to limit the discussion to vertebrate species and specialization of the right hemisphere for social behaviour could be discussed (see Rosa Salva et al, 2012, Comparative Cognition and Behavior 7, 110-138).

609: I am reminded here of the “hand waving” of lizards. Perhaps the apparent absence of gestural communication in non-primates is simply a matter of not using the same nomenclature or terms to describe it.

Author Response

Reviewer 2:

147: Something is missing inside the brackets.

→ We actually use the symbol “[...]” to indicate a cut in the citation.

165: Change ‘dependent from’ to ‘dependent on’.

→ Thank you for notifying it! We corrected it.

→ Thank you for notifying us of this mistake: one of the references was misplaced. We intended to cite the Brown & Magat paper from 2011 (Biology Letters) in which they found out that “eye preferences explained 99 per cent of the variation in foot use in Australian parrots” (when investigating food items). We fixed it.

We also added a paragraph about the new study you pointed out, thank you for this suggestion (L.230-246):

“Regarding non-primate species, brain lateralization in Australian parrots parrots' footedness is correlated with eye lateralization for discriminating food items, supporting - according to the authors - a functional explanation for the evolution of handedness in vertebratesis highly correlated with “hand” (i.e., foot) preference for manipulating food items (Figure1) [77]. A recent study investigated the association between brain size and parrots’ (psittacine) foot preference [78]. It has been shown that cerebral lateralization enhances the brain capacity by allowing parallel processing of sensory information (e.g., to forage efficiently while remaining vigilant for predators) [26]. As the Australian parrot’s species known for having foot preferences also have better ability to perform certain manipulative and cognitive tasks compared to species with no foot preference [79], Rogers and Kaplan and Rogers [78] asked the following question: «Do species with footedness have larger brains, or is footedness a way of compensating for having a smaller brain? » (p.2). The authors found in several Australian parrots that species with larger brains (i.e., absolute brain mass) have stronger foot preference and that left-footedness is stronger in species with a larger brain. Moreover, the authors found foot preference to be associated with the size of a brain area (i.e., the nidopallium) recruited for higher cognitive tasks, so that species with stronger left-foot preferences have larger brains, with a larger volume of the nidopallium (compared to the whole brain) [78].”

239: Change claws to claw.

→ Thank you ! We corrected it.

248: Change take to taking.

→ Thank you ! We corrected it.

→ Thank you for this suggestion. We added this example with the corresponding reference (L.514-519):

“This idea is strengthened by the fact that a positive relation was found between right-handedness and approach motivations in captive chimpanzees in an experimental context [159]. A similar association was observed in Geoffroy’s marmosets (Callithrix geoffroyi), in which right-handed individuals presented to novel objects seemed less fearful and exhibited more frequent approach behaviors than left-handed subjects [160,161]. “

450: Change ‘than in primates’ to ‘as in primates’.

→ Thank you ! We corrected it.

→ Thank you for this comment. We agree that the behavioral lateralizations observed in fruit flies might not be homologous with those observed in vertebrates. We thus added sentences to explain how this example is rather interesting regarding the evolutionary constraints which shape forelimb laterality in animals, and may lead to such evolutionary convergence (L.599-603):

“This lateralization in insects may not be homologous (i.e., be inherited from a common ancestor) to the left-hand / right-hemispheric preference observed in vertebrates for socially-directed actions, hence it reflects the possibly ubiquitous nature of the constraints that social interactions represent on the lateralization of social animals’ behaviors [192].”

Moreover, we added sentences before this paragraph, in order to discuss the involvement of the right hemisphere in social behavior (L.584-588):

“The right hemisphere of vertebrates seems specialized for the processing of social information, notably for the purpose of emotional signal perception [16,141,142] or individual recognition [190]. This may result in a higher involvement of this hemisphere for performing manual actions directed towards conspecifics compared to manual actions directed to inanimate objects, resulting in a higher use of the left side of the body.”

→ This is indeed an interesting remark. There is a wide diversity of definitions for manual gestures, which unfortunately lead to difficulties to make reliable interspecies comparisons. We made the choice here to focus on the primate clade regarding gestural laterality and its potential involvement in human language evolution, given that the operational definitions of gestures used for these species make them more comparable with human communication. However, such gestural signals might exist in other species, but has not been, as far of our knowledge, described with the same criteria.