The evolution and biological correlates of hand preferences in anthropoid primates
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Evaluation Summary:
This paper combines new and previously generated data on hand preference to show that hand preference strength, but not direction, is predicted by ecology and phylogeny across primates. By drawing on the most expansive data set to date on experimentally determined hand preference, it calls existing hypotheses on the evolution of hand preference into question and shows that the strength of lateralization in humans is uniquely extreme. Its results are of interest to evolutionary anthropologists, primatologists, and evolutionary morphologists. However, concerns about intraspecific variation and the accuracy of handedness estimates for poorly sampled species are incompletely addressed by the manuscript in its current form.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their names with the authors.)
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Abstract
The evolution of human right-handedness has been intensively debated for decades. Manual lateralization patterns in non-human primates have the potential to elucidate evolutionary determinants of human handedness, but restricted species samples and inconsistent methodologies have so far limited comparative phylogenetic studies. By combining original data with published literature reports, we assembled data on hand preferences for standardized object manipulation in 1786 individuals from 38 species of anthropoid primates, including monkeys, apes, and humans. Based on that, we employ quantitative phylogenetic methods to test prevalent hypotheses on the roles of ecology, brain size, and tool use in primate handedness evolution. We confirm that human right-handedness represents an unparalleled extreme among anthropoids and found taxa displaying population-level handedness to be rare. Species-level direction of manual lateralization was largely uniform among non-human primates and did not strongly correlate with any of the selected biological predictors, nor with phylogeny. In contrast, we recovered highly variable patterns of hand preference strength, which show signatures of both ecology and phylogeny. In particular, terrestrial primates tend to display weaker hand preferences than arboreal species. These results challenge popular ideas on primate handedness evolution, including the postural origins hypothesis. Furthermore, they point to a potential adaptive benefit of disparate lateralization strength in primates, a measure of hand preference that has often been overlooked in the past. Finally, our data show that human lateralization patterns do not align with trends found among other anthropoids, suggesting that unique selective pressures gave rise to the unusual hand preferences of our species.
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Author Response
Reviewer 1
This is an interesting manuscript that has the potential to answer questions about a controversial topic in evolutionary biology - the evolutionary patterns and drivers of hand preferences in humans and nonhuman primates. To accomplish this, the authors generate new data and gather an impressive amount of published data across many anthropoid species, and test for the effects of ecology (terrestrial vs. arboreal), brain size, and tool use on handedness using phylogenetically informed statistical analyses. They find that humans represent an extreme among the species sampled, that direction of handedness was not correlated with any of the predictors tested, and that strength of handedness was higher among arboreal species.
Although phylogenetic modeling (which accounts for relatedness between species) is …
Author Response
Reviewer 1
This is an interesting manuscript that has the potential to answer questions about a controversial topic in evolutionary biology - the evolutionary patterns and drivers of hand preferences in humans and nonhuman primates. To accomplish this, the authors generate new data and gather an impressive amount of published data across many anthropoid species, and test for the effects of ecology (terrestrial vs. arboreal), brain size, and tool use on handedness using phylogenetically informed statistical analyses. They find that humans represent an extreme among the species sampled, that direction of handedness was not correlated with any of the predictors tested, and that strength of handedness was higher among arboreal species.
Although phylogenetic modeling (which accounts for relatedness between species) is implemented in the primary analyses reported in this paper (e.g., testing the effects of ecology, brain size, and tool use on handedness), this is not the case for some other analyses (e.g., testing the effects of sex, age, and subgroup on handedness). This represents one potential area of improvement.
Overall, the manuscript is very well-written and the new data gathered is impressive. This work is critical for our understanding of the role of handedness in primate evolution.
Thank you for your positive feedback on our manuscript. We appreciate your in-depth review and answer the queries point by point below.
Reviewer 2
The present paper presents an impressive meta-analyze on handedness for a bimanual coordinated tube task (which has been considered in the literature as a robust and reliable task to assess hand preference in nonhuman primates) in about 38 primate species including new sets of data collected by the authors themselves. The work that has been done to compile exhaustively all the available data is considerable and very valuable. The authors presented also, in the introduction, a very nice and useful review and clarification of the different existing evolutionary theories that have previously been proposed in the literature to try to interpret the discrepancy of findings reported across primate species. For instance, different hypotheses are contrasted such as (1) the one highlighting the role of the tool use emergence, (2) the one highlighting the role of brain size, and (3) the postural origin hypothesis (i.e., the predominance of right-handedness evolved with the emergence of anthropoid primates, regardless of ecology), or (4) the "novel (corrected) postural origin hypothesis" that I have been proposed with coauthors (i.e., the predominance of right-handedness for bimanual actions is related to terrestrial ecology whereas predominance of left-handedness is related to arboreal ecology, regardless of phylogeny). Such an exhaustive review of handedness data in bimanual tasks across the largest comparative approach ever done allows the authors to evaluate those several hypotheses by testing the effect of their related factors (phylogeny, ecology, emergence of tool use, brain size) on the pattern of handedness. Using quantitative phylogenetic methods, the authors found that none of those factors are actually predictive of the direction of population-level handedness in non-human primates questioning seriously each of those existing hypotheses.
Thank you very much for the positive evaluation of our manuscript and the additional statistical work behind it!
I believe this large review and study is very important and relevant for investigating the evolution of handedness, although I questioned the strong claim (supported by the lake of findings resulting from the quantitative phylogenetic methods) that the dichotomy of arboreal versus terrestrial lifestyle has nothing to do with the direction of population-level handedness in a non-human primate. A significant difference in direction of handedness between these two lifestyles seems still robust when considering clade-level (not species-level), an effect driven by overrepresented species for which high sample sizes have been included. The question of sample size and statistical power for evaluating and inferring population-level of handedness is thus a potential critical factor that should be discussed for evaluating different evolutionary theories. It might be indeed not excluded that the lake of results at the species level is equivocal given the lack of statistical power in most species (related to a poor sample size of subjects).
Nevertheless, I congratulate the authors for this amazing and considerable work. I had such a pleasure reading it and hope my comments and questions were useful.
Thank you very much.
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Evaluation Summary:
This paper combines new and previously generated data on hand preference to show that hand preference strength, but not direction, is predicted by ecology and phylogeny across primates. By drawing on the most expansive data set to date on experimentally determined hand preference, it calls existing hypotheses on the evolution of hand preference into question and shows that the strength of lateralization in humans is uniquely extreme. Its results are of interest to evolutionary anthropologists, primatologists, and evolutionary morphologists. However, concerns about intraspecific variation and the accuracy of handedness estimates for poorly sampled species are incompletely addressed by the manuscript in its current form.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; …
Evaluation Summary:
This paper combines new and previously generated data on hand preference to show that hand preference strength, but not direction, is predicted by ecology and phylogeny across primates. By drawing on the most expansive data set to date on experimentally determined hand preference, it calls existing hypotheses on the evolution of hand preference into question and shows that the strength of lateralization in humans is uniquely extreme. Its results are of interest to evolutionary anthropologists, primatologists, and evolutionary morphologists. However, concerns about intraspecific variation and the accuracy of handedness estimates for poorly sampled species are incompletely addressed by the manuscript in its current form.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their names with the authors.)
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Reviewer #1 (Public Review):
This is an interesting manuscript that has the potential to answer questions about a controversial topic in evolutionary biology - the evolutionary patterns and drivers of hand preferences in humans and nonhuman primates. To accomplish this, the authors generate new data and gather an impressive amount of published data across many anthropoid species, and test for the effects of ecology (terrestrial vs. arboreal), brain size, and tool use on handedness using phylogenetically informed statistical analyses. They find that humans represent an extreme among the species sampled, that direction of handedness was not correlated with any of the predictors tested, and that strength of handedness was higher among arboreal species.
Although phylogenetic modeling (which accounts for relatedness between species) is …
Reviewer #1 (Public Review):
This is an interesting manuscript that has the potential to answer questions about a controversial topic in evolutionary biology - the evolutionary patterns and drivers of hand preferences in humans and nonhuman primates. To accomplish this, the authors generate new data and gather an impressive amount of published data across many anthropoid species, and test for the effects of ecology (terrestrial vs. arboreal), brain size, and tool use on handedness using phylogenetically informed statistical analyses. They find that humans represent an extreme among the species sampled, that direction of handedness was not correlated with any of the predictors tested, and that strength of handedness was higher among arboreal species.
Although phylogenetic modeling (which accounts for relatedness between species) is implemented in the primary analyses reported in this paper (e.g., testing the effects of ecology, brain size, and tool use on handedness), this is not the case for some other analyses (e.g., testing the effects of sex, age, and subgroup on handedness). This represents one potential area of improvement.
Overall, the manuscript is very well-written and the new data gathered is impressive. This work is critical for our understanding of the role of handedness in primate evolution.
-
Reviewer #2 (Public Review):
The present paper presents an impressive meta-analyze on handedness for a bimanual coordinated tube task (which has been considered in the literature as a robust and reliable task to assess hand preference in nonhuman primates) in about 38 primate species including new sets of data collected by the authors themselves. The work that has been done to compile exhaustively all the available data is considerable and very valuable. The authors presented also, in the introduction, a very nice and useful review and clarification of the different existing evolutionary theories that have previously been proposed in the literature to try to interpret the discrepancy of findings reported across primate species. For instance, different hypotheses are contrasted such as (1) the one highlighting the role of the tool use …
Reviewer #2 (Public Review):
The present paper presents an impressive meta-analyze on handedness for a bimanual coordinated tube task (which has been considered in the literature as a robust and reliable task to assess hand preference in nonhuman primates) in about 38 primate species including new sets of data collected by the authors themselves. The work that has been done to compile exhaustively all the available data is considerable and very valuable. The authors presented also, in the introduction, a very nice and useful review and clarification of the different existing evolutionary theories that have previously been proposed in the literature to try to interpret the discrepancy of findings reported across primate species. For instance, different hypotheses are contrasted such as (1) the one highlighting the role of the tool use emergence, (2) the one highlighting the role of brain size, and (3) the postural origin hypothesis (i.e., the predominance of right-handedness evolved with the emergence of anthropoid primates, regardless of ecology), or (4) the "novel (corrected) postural origin hypothesis" that I have been proposed with coauthors (i.e., the predominance of right-handedness for bimanual actions is related to terrestrial ecology whereas predominance of left-handedness is related to arboreal ecology, regardless of phylogeny). Such an exhaustive review of handedness data in bimanual tasks across the largest comparative approach ever done allows the authors to evaluate those several hypotheses by testing the effect of their related factors (phylogeny, ecology, emergence of tool use, brain size) on the pattern of handedness. Using quantitative phylogenetic methods, the authors found that none of those factors are actually predictive of the direction of population-level handedness in non-human primates questioning seriously each of those existing hypotheses.
I believe this large review and study is very important and relevant for investigating the evolution of handedness, although I questioned the strong claim (supported by the lake of findings resulting from the quantitative phylogenetic methods) that the dichotomy of arboreal versus terrestrial lifestyle has nothing to do with the direction of population-level handedness in a non-human primate. A significant difference in direction of handedness between these two lifestyles seems still robust when considering clade-level (not species-level), an effect driven by overrepresented species for which high sample sizes have been included. The question of sample size and statistical power for evaluating and inferring population-level of handedness is thus a potential critical factor that should be discussed for evaluating different evolutionary theories. It might be indeed not excluded that the lake of results at the species level is equivocal given the lack of statistical power in most species (related to a poor sample size of subjects).
Nevertheless, I congratulate the authors for this amazing and considerable work. I had such a pleasure reading it and hope my comments and questions were useful.
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