The evolution and biological correlates of hand preferences in anthropoid primates
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
36454207
PubMed Central
PMC9714969
DOI
10.7554/elife.77875
PII: 77875
Knihovny.cz E-zdroje
- Klíčová slova
- Cercopithecoidea, Hominoidea, Platyrrhini, evolutionary biology, handedness, laterality, motor control, neuroscience,
- MeSH
- ekologie * MeSH
- funkční lateralita genetika MeSH
- fylogeneze MeSH
- Haplorrhini MeSH
- lidé MeSH
- primáti * MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
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.
About 90% of humans are right-handed. While it is known that handedness is caused by certain brain regions that are specialized in one of the two hemispheres, it is not clear how this evolved or why right-handedness dominates. Several hypotheses have been proposed to explain this extreme preference, including the use of tools, the larger size of the human brain, and the fact that humans live primarily on the ground. Many researchers have regarded the extreme population-wide preference for using the right hand as being uniquely human. However, handedness had not been studied in a standardized manner across a wide range of primates. To fill this gap in our knowledge and understand how handedness may have evolved in monkeys and apes, Caspar et al. used existing data and new experimental observations to create a large dataset of hand preference. This dataset illustrates how approximately 1800 primates across 38 species retrieve mashed food from a tube (or pieces of paper in the case of humans). Similar to humans, some species of monkey only had small proportions of ambidextrous individuals. However, no species had an extreme preference for using one specific hand the way humans do. Interestingly, Caspar et al. found that the presence of tool use as well as brain size were not associated with the degree of handedness in species. However, ground-living primates tended to show weaker individual preferences for a specific hand than tree-living species, with humans being a notable exception to the trend. These findings confirm that humans do exhibit exceptional right-handedness, being unique among primates. While the results cannot explain the cause of this behaviour, they do help to rule out some of the theories that aim to explain how this preference evolved. This will be of interest to researchers studying the origins of human behaviour as well as the emergence of asymmetries in the brain.
Department of General Zoology University of Duisburg Essen Essen Germany
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Amunts K, Schlaug G, Schleicher A, Steinmetz H, Dabringhaus A, Roland PE, Zilles K. Asymmetry in the human motor cortex and handedness. NeuroImage. 1996;4:216–222. doi: 10.1006/nimg.1996.0073. PubMed DOI
Ankel-Simons F, Rasmussen DT. Diurnality, nocturnality, and the evolution of primate visual systems. American Journal of Physical Anthropology. 2008;Suppl 47:100–117. doi: 10.1002/ajpa.20957. PubMed DOI
Annett M. Handedness and Brain Asymmetry: The Right Shift Theory. Hove: Psychology Press; 2002.
Ardesch DJ, Scholtens LH, de Lange SC, Roumazeilles L, Khrapitchev AA, Preuss TM, Rilling JK, Mars RB, van den Heuvel MP. Scaling principles of white matter connectivity in the human and nonhuman primate brain. Cerebral Cortex. 2021;32:2831–2842. doi: 10.1093/cercor/bhab384. PubMed DOI PMC
Arnold C, Matthews LJ, Nunn CL. The 10ktrees website: a new online resource for primate phylogeny. Evolutionary Anthropology. 2010;19:114–118. doi: 10.1002/evan.20251. DOI
Barrett RLC, Dawson M, Dyrby TB, Krug K, Ptito M, D’Arceuil H, Croxson PL, Johnson PJ, Howells H, Forkel SJ, Dell’Acqua F, Catani M. Differences in frontal network anatomy across primate species. The Journal of Neuroscience. 2020;40:2094–2107. doi: 10.1523/JNEUROSCI.1650-18.2019. PubMed DOI PMC
Barton K. MuMIn: multi-model inference. 1.43.17R Package. 2020 https://CRAN.R-project.org/package=MuMIn
Batist CH, Mayhew JA. Lateralization in seven lemur species when presented with a novel cognitive task. American Journal of Physical Anthropology. 2020;172:270–279. doi: 10.1002/ajpa.24037. PubMed DOI
Becker Y, Claidière N, Margiotoudi K, Marie D, Roth M, Nazarian B, Anton JL, Coulon O, Meguerditchian A. Broca’s cerebral asymmetry reflects gestural communication’s lateralisation in monkeys (Papio anubis) eLife. 2022;11:e70521. doi: 10.7554/eLife.70521. PubMed DOI PMC
Blois-Heulin C, Bernard V, Bec P. Postural effect on manual laterality in different tasks in captive grey-cheeked mangabey (Lophocebus albigena) Journal of Comparative Psychology. 2007;121:205–213. doi: 10.1037/0735-7036.121.2.205. PubMed DOI
Bürkner P. Brms: an R package for Bayesian multilevel models using Stan. Journal of Statistical Software. 2017;80:1–28. doi: 10.18637/jss.v080.i01. DOI
Canteloup C, Vauclair J, Meunier H. Hand preferences on unimanual and bimanual tasks in tonkean macaques (Macaca tonkeana) American Journal of Physical Anthropology. 2013;152:315–321. doi: 10.1002/ajpa.22342. PubMed DOI
Cashmore L, Uomini N, Chapelain A. The evolution of handedness in humans and great apes: a review and current issues. Journal of Anthropological Sciences = Rivista Di Antropologia. 2008;86:7–35. PubMed
Caspar KR, Mader L, Pallasdies F, Lindenmeier M, Begall S. Captive gibbons (Hylobatidae) use different referential cues in an object-choice task: insights into lesser ape cognition and manual laterality. PeerJ. 2018;6:e5348. doi: 10.7717/peerj.5348. PubMed DOI PMC
Chatagny P, Badoud S, Kaeser M, Gindrat A-D, Savidan J, Fregosi M, Moret V, Roulin C, Schmidlin E, Rouiller EM. Distinction between hand dominance and hand preference in primates: a behavioral investigation of manual dexterity in nonhuman primates (macaques) and human subjects. Brain and Behavior. 2013;3:575–595. doi: 10.1002/brb3.160. PubMed DOI PMC
Cochet H, Vauclair J. Hand preferences in human adults: non-communicative actions versus communicative gestures. Cortex; a Journal Devoted to the Study of the Nervous System and Behavior. 2012;48:1017–1026. doi: 10.1016/j.cortex.2011.03.016. PubMed DOI
Corballis MC. Straw monkeys. Behavioral and Brain Sciences. 1987;10:269–270. doi: 10.1017/S0140525X00047762. DOI
Corballis MC. The Lopsided Ape: Evolution of the Generative Mind. Oxford University Press; 1991.
Coren S, Porac C. Fifty centuries of right-handedness: the historical record. Science. 1977;198:631–632. doi: 10.1126/science.335510. PubMed DOI
Cubí M, Llorente M. Hand preference for a bimanual coordinated task in captive hatinh langurs (Trachypithecus hatinhensis) and grey-shanked douc langurs (Pygathrix cinerea) Behavioural Processes. 2021;187:104393. doi: 10.1016/j.beproc.2021.104393. PubMed DOI
Dadda M, Cantalupo C, Hopkins WD. Further evidence of an association between handedness and neuroanatomical asymmetries in the primary motor cortex of chimpanzees (Pan troglodytes) Neuropsychologia. 2006;44:2582–2586. doi: 10.1016/j.neuropsychologia.2006.03.037. PubMed DOI PMC
De Andrade AC, Sousa AB. Hand preferences and differences in extractive foraging in seven capuchin monkey species. American Journal of Primatology. 2018;80:e22901. doi: 10.1002/ajp.22901. PubMed DOI
Diamond AC, McGrew WC. True handedness in the cotton-top tamarin (Saguinus oedipus)? Primates. 1994;35:69–77. doi: 10.1007/BF02381487. DOI
Fan P, Liu C, Chen H, Liu X, Zhao D, Zhang J, Liu D. Preliminary study on hand preference in captive northern white-cheeked gibbons (Nomascus leucogenys) Primates; Journal of Primatology. 2017;58:75–82. doi: 10.1007/s10329-016-0573-8. PubMed DOI
Faurie C, Schiefenhövel W, le Bomin S, Billiard S, Raymond M. Variation in the frequency of left‐handedness in traditional societies. Current Anthropology. 2005;46:142–147. doi: 10.1086/427101. DOI
Fitch WT, Braccini SN. Primate laterality and the biology and evolution of human handedness: a review and synthesis. Annals of the New York Academy of Sciences. 2013;1288:70–85. doi: 10.1111/nyas.12071. PubMed DOI
Freckleton RP, Harvey PH, Pagel M. Phylogenetic analysis and comparative data: a test and review of evidence. The American Naturalist. 2002;160:712–726. doi: 10.1086/343873. PubMed DOI
Frost GT. Tool behavior and the origins of laterality. Journal of Human Evolution. 1980;9:447–459. doi: 10.1016/0047-2484(80)90002-0. DOI
Gebo DL. Vertical clinging and leaping revisited: vertical support use as the ancestral condition of strepsirrhine primates. American Journal of Physical Anthropology. 2011;146:323–335. doi: 10.1002/ajpa.21595. PubMed DOI
Giljov A, Karenina K, Ingram J, Malashichev Y. Parallel emergence of true handedness in the evolution of marsupials and placentals. Current Biology. 2015;25:1878–1884. doi: 10.1016/j.cub.2015.05.043. PubMed DOI
Häberling IS, Corballis MC. Cerebellar asymmetry, cortical asymmetry and handedness: two independent networks. Laterality. 2016;21:397–414. doi: 10.1080/1357650X.2015.1110161. PubMed DOI
Harvey PH, Clutton-Brock TH. Life history variation in primates. Evolution; International Journal of Organic Evolution. 1985;39:559–581. doi: 10.1111/j.1558-5646.1985.tb00395.x. PubMed DOI
Hecht EE, Gutman DA, Khreisheh N, Taylor SV, Kilner J, Faisal AA, Bradley BA, Chaminade T, Stout D. Acquisition of paleolithic toolmaking abilities involves structural remodeling to inferior frontoparietal regions. Brain Structure & Function. 2015a;220:2315–2331. doi: 10.1007/s00429-014-0789-6. PubMed DOI
Hecht EE, Gutman DA, Bradley BA, Preuss TM, Stout D. Virtual dissection and comparative connectivity of the superior longitudinal fasciculus in chimpanzees and humans. NeuroImage. 2015b;108:124–137. doi: 10.1016/j.neuroimage.2014.12.039. PubMed DOI PMC
Hopkins WD. Hand preferences for a coordinated bimanual task in 110 chimpanzees (Pan troglodytes): cross-sectional analysis. Journal of Comparative Psychology. 1995;109:291–297. doi: 10.1037/0735-7036.109.3.291. PubMed DOI
Hopkins WD, Fernandez-Carriba S, Wesley MJ, Hostetter A, Pilcher D, Poss S. The use of bouts and frequencies in the evaluation of hand preferences for a coordinated bimanual task in chimpanzees (Pan troglodytes): an empirical study comparing two different indices of laterality. Journal of Comparative Psychology. 2001;115:294–299. doi: 10.1037//0735-7036.115.3.294. PubMed DOI PMC
Hopkins WD, Cantalupo C. Handedness in chimpanzees (Pan troglodytes) is associated with asymmetries of the primary motor cortex but not with homologous language areas. Behavioral Neuroscience. 2004;118:1176–1183. doi: 10.1037/0735-7044.118.6.1176. PubMed DOI PMC
Hopkins WD, Phillips KA, Bania A, Calcutt SE, Gardner M, Russell J, Schaeffer J, Lonsdorf EV, Ross SR, Schapiro SJ. Hand preferences for coordinated bimanual actions in 777 great apes: implications for the evolution of handedness in hominins. Journal of Human Evolution. 2011;60:605–611. doi: 10.1016/j.jhevol.2010.12.008. PubMed DOI PMC
Hopkins WD. Neuroanatomical asymmetries and handedness in chimpanzees (Pan troglodytes): a case for continuity in the evolution of hemispheric specialization. Annals of the New York Academy of Sciences. 2013a;1288:17–35. doi: 10.1111/nyas.12109. PubMed DOI PMC
Hopkins WD, Adams MJ, Weiss A. Genetic and environmental contributions to the expression of handedness in chimpanzees (Pan troglodytes) Genes, Brain, and Behavior. 2013a;12:446–452. doi: 10.1111/gbb.12044. PubMed DOI PMC
Hopkins WD. Comparing human and nonhuman primate handedness: challenges and a modest proposal for consensus. Developmental Psychobiology. 2013b;55:621–636. doi: 10.1002/dev.21139. PubMed DOI PMC
Hopkins WD, Gardner M, Mingle M, Reamer L, Schapiro SJ. Within- and between-task consistency in hand use as a means of characterizing hand preferences in captive chimpanzees (Pan troglodytes) Journal of Comparative Psychology. 2013b;127:380–391. doi: 10.1037/a0031071. PubMed DOI PMC
Kaplan G, Rogers LJ. Brain size associated with foot preferences in Australian parrots. Symmetry. 2021;13:867. doi: 10.3390/sym13050867. DOI
Karolis VR, Corbetta M, Thiebaut de Schotten M. The architecture of functional lateralisation and its relationship to callosal connectivity in the human brain. Nature Communications. 2019;10:1417. doi: 10.1038/s41467-019-09344-1. PubMed DOI PMC
Kimura D. In: Neurobiology of Social Communication in Primates: An Evolutionary Perspective. Paleigh HDSM, editor. Cambridge: Academic Press; 1979. Neuromotor mechanisms in the evolution of human communication; pp. 1197–1220. DOI
Kitchener AC, Meloro C, Williams TM. In: The Biology and Conservation of Wild Musteloids. Macdonald DW, Newman C, Harrington L, editors. Oxford: Oxford University Press; 2017. Form and function of the musteloids; pp. 98–135. DOI
Kong XZ, Mathias SR, Guadalupe T, Glahn DC, Franke B, Crivello F, Tzourio-Mazoyer N, Fisher SE, Thompson PM, Francks C, ENIGMA Laterality Working Group Mapping cortical brain asymmetry in 17,141 healthy individuals worldwide via the enigma consortium. PNAS. 2018;115:E5154–E5163. doi: 10.1073/pnas.1718418115. PubMed DOI PMC
Krasheninnikova A, Chow PKY, von Bayern AMP. Comparative cognition: practical shortcomings and some potential ways forward. Canadian Journal of Experimental Psychology = Revue Canadienne de Psychologie Experimentale. 2020;74:160–169. doi: 10.1037/cep0000204. PubMed DOI
Laska M. A study of correlates of hand preferences in squirrel monkeys (Saimiri sciureus) Primates. 1996;37:457–465. doi: 10.1007/BF02381379. DOI
Laurence A, Wallez C, Blois-Heulin C. Task complexity, posture, age, sex: which is the main factor influencing manual laterality in captive Cercocebus torquatus torquatus? Laterality. 2011;16:586–606. doi: 10.1080/1357650X.2010.501338. PubMed DOI
Lilak AL, Phillips KA. Consistency of hand preference across low-level and high-level tasks in capuchin monkeys (Cebus apella) American Journal of Primatology. 2008;70:254–260. doi: 10.1002/ajp.20485. PubMed DOI
Lima MGM, Silva-Júnior JDS, Černý D, Buckner JC, Aleixo A, Chang J, Zheng J, Alfaro ME, Martins A, Di Fiore A, Boubli JP, Lynch Alfaro JW. A phylogenomic perspective on the robust capuchin monkey (Sapajus) radiation: first evidence for extensive population admixture across south america. Molecular Phylogenetics and Evolution. 2018;124:137–150. doi: 10.1016/j.ympev.2018.02.023. PubMed DOI
Lozano M, Estalrrich A, Bondioli L, Fiore I, Bermúdez de Castro J-M, Arsuaga JL, Carbonell E, Rosas A, Frayer DW. Right-handed fossil humans. Evolutionary Anthropology. 2017;26:313–324. doi: 10.1002/evan.21554. PubMed DOI
MacLean EL, Matthews LJ, Hare BA, Nunn CL, Anderson RC, Aureli F, Brannon EM, Call J, Drea CM, Emery NJ, Haun DBM, Herrmann E, Jacobs LF, Platt ML, Rosati AG, Sandel AA, Schroepfer KK, Seed AM, Tan J, van Schaik CP, Wobber V. How does cognition evolve? Phylogenetic comparative psychology. Animal Cognition. 2012;15:223–238. doi: 10.1007/s10071-011-0448-8. PubMed DOI PMC
MacNeilage PF, Studdert-Kennedy MG, Lindblom B. Primate handedness reconsidered. Behavioral and Brain Sciences. 1987;10:247–263. doi: 10.1017/S0140525X00047695. DOI
MacNeilage PF. In: In The Evolution of Hemispheric Specialization in Primates. Hopkins WD, editor. Oxford: Elsevier; 2007. Present status of the postural origins theory; pp. 59–91. DOI
Maille A, Belbeoc’h C, Rossard A, Bec P, Blois-Heulin C. Which are the features of the tube task that make it so efficient in detecting manual asymmetries? an investigation in two cercopithecine species (Cercopithecus neglectus and Cercocebus torquatus) Journal of Comparative Psychology. 2013;127:436–444. doi: 10.1037/a0032227. PubMed DOI
ManyPrimates. Altschul DM, Beran MJ, Bohn M, Caspar KR, Fichtel C, Försterling M, Grebe N, Hernandez-Aguilar RA, Kwok SC, Rodrigo AM, Proctor D, Sanchez-Amaro A, Simpson EA, Szabelska A, Taylor D, van der Mescht J, Völter C, Watzek J. Collaborative open science as a way to reproducibility and new insights in primate cognition research. Japanese Psychological Review. 2019;63:205–220.
Marchant LF, McGrew WC. Handedness is more than laterality: lessons from chimpanzees. Annals of the New York Academy of Sciences. 2013;1288:1–8. doi: 10.1111/nyas.12062. PubMed DOI
Margiotoudi K, Marie D, Claidière N, Coulon O, Roth M, Nazarian B, Lacoste R, Hopkins WD, Molesti S, Fresnais P, Anton JL, Meguerditchian A. Handedness in monkeys reflects hemispheric specialization within the central sulcus: an in vivo MRI study in right- and left-handed olive baboons. Cortex; a Journal Devoted to the Study of the Nervous System and Behavior. 2019;118:203–211. doi: 10.1016/j.cortex.2019.01.001. PubMed DOI
Meguerditchian A., Donnot J, Molesti S, Francioly R, Vauclair J. Sex difference in squirrel monkeys’ handedness for unimanual and bimanual coordinated tasks. Animal Behaviour. 2012;83:635–643. doi: 10.1016/j.anbehav.2011.12.005. DOI
Meguerditchian A., Vauclair J, Hopkins WD. On the origins of human handedness and language: a comparative review of hand preferences for bimanual coordinated actions and gestural communication in nonhuman primates. Developmental Psychobiology. 2013;55:637–650. doi: 10.1002/dev.21150. PubMed DOI
Meguerditchian A, Phillips KA, Chapelain A, Mahovetz LM, Milne S, Stoinski T, Bania A, Lonsdorf E, Schaeffer J, Russell J, Hopkins WD. Handedness for unimanual grasping in 564 great apes: the effect on grip morphology and a comparison with hand use for a bimanual coordinated task. Frontiers in Psychology. 2015;6:1794. doi: 10.3389/fpsyg.2015.01794. PubMed DOI PMC
Mittermeier RA, Rylands AB, Wilson DE. Handbook of the Mammals of the World: 3. Primates. Lynx Ediciones; 2013.
Morales-Jimenez AL, Disotell T, Di Fiore A. Revisiting the phylogenetic relationships, biogeography, and taxonomy of spider monkeys (genus Ateles) in light of new molecular data. Molecular Phylogenetics and Evolution. 2015;82 Pt B:467–483. doi: 10.1016/j.ympev.2014.09.019. PubMed DOI
Morino L, Uchikoshi M, Bercovitch F, Hopkins WD, Matsuzawa T. Tube task hand preference in captive hylobatids. Primates; Journal of Primatology. 2017;58:403–412. doi: 10.1007/s10329-017-0605-z. PubMed DOI
Motes Rodrigo A, Ramirez Torres CE, Hernandez Salazar LT, Laska M. Hand preferences in two unimanual and two bimanual coordinated tasks in the black-handed spider monkey (Ateles geoffroyi) Journal of Comparative Psychology. 2018;132:220–229. doi: 10.1037/com0000110. PubMed DOI
Musgrave S, Sanz C. In: The International Encyclopedia of Anthropology. Callan H, editor. WIley; 2018. Tool use in nonhuman primates; pp. 1–20. DOI
Nelson EL, Boeving ER. Precise digit use increases the expression of handedness in Colombian spider monkeys (Ateles fusciceps rufiventris) American Journal of Primatology. 2015;77:1253–1262. doi: 10.1002/ajp.22478. PubMed DOI
Ocklenburg S, Beste C, Arning L, Peterburs J, Güntürkün O. The ontogenesis of language lateralization and its relation to handedness. Neuroscience and Biobehavioral Reviews. 2014;43:191–198. doi: 10.1016/j.neubiorev.2014.04.008. PubMed DOI
Papademetriou E, Sheu CF, Michel GF. A meta-analysis of primate hand preferences, particularly for reaching. Journal of Comparative Psychology. 2005;119:33–48. doi: 10.1037/0735-7036.119.1.33. PubMed DOI
Paradis E, Schliep K, Schwartz R. Ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics. 2019;35:526–528. doi: 10.1093/bioinformatics/bty633. PubMed DOI
Phillips KA, Sherwood CC. Primary motor cortex asymmetry is correlated with handedness in capuchin monkeys (Cebus apella) Behavioral Neuroscience. 2005;119:1701–1704. doi: 10.1037/0735-7044.119.6.1701. PubMed DOI
Phillips KA, Sherwood CC, Lilak AL. Corpus callosum morphology in capuchin monkeys is influenced by sex and handedness. PLOS ONE. 2007;2:e792. doi: 10.1371/journal.pone.0000792. PubMed DOI PMC
Pinheiro J. Nlme: linear and nonlinear mixed effects models. 3.1-148R Package Version. 2020 https://CRAN.R-project.org/package=nlme
Prieur J, Lemasson A, Barbu S, Blois‐Heulin C, Bshary R. History, development and current advances concerning the evolutionary roots of human right‐handedness and language: brain lateralisation and manual laterality in non‐human primates. Ethology. 2019;125:1–28. doi: 10.1111/eth.12827. DOI
Ramayya AG, Glasser MF, Rilling JK. A DTI investigation of neural substrates supporting tool use. Cerebral Cortex. 2010;20:507–516. doi: 10.1093/cercor/bhp141. PubMed DOI
Rasmussen DT, Nekaris KA. Evolutionary history of lorisiform primates. Folia Primatologica; International Journal of Primatology. 1998;69 Suppl 1:250–285. doi: 10.1159/000052716. PubMed DOI
Raymond M, Pontier D. Is there geographical variation in human handedness? Laterality. 2004;9:35–51. doi: 10.1080/13576500244000274. PubMed DOI
R Development Core Team . Vienna, Austria: R Foundation for Statistical Computing; 2020. https://www.R-project.org/
Regaiolli B, Spiezio C, Hopkins WD. Hand preference on unimanual and bimanual tasks in strepsirrhines: the case of the ring-tailed lemur (Lemur catta) American Journal of Primatology. 2016;78:851–860. doi: 10.1002/ajp.22549. PubMed DOI
Regaiolli B, Spiezio C, Hopkins WD. Hand preference on unimanual and bimanual tasks in barbary macaques (Macaca sylvanus) American Journal of Primatology. 2018;80:e22745. doi: 10.1002/ajp.22745. PubMed DOI
Revell LJ. Phytools: an R package for phylogenetic comparative biology (and other things) Methods in Ecology and Evolution. 2012;3:217–223. doi: 10.1111/j.2041-210X.2011.00169.x. DOI
Richards G, Beking T, Kreukels BPC, Geuze RH, Beaton AA, Groothuis T. An examination of the influence of prenatal sex hormones on handedness: literature review and amniotic fluid data. Hormones and Behavior. 2021;129:104929. doi: 10.1016/j.yhbeh.2021.104929. PubMed DOI
Rilling JK, Insel TR. Differential expansion of neural projection systems in primate brain evolution. Neuroreport. 1999;10:1453–1459. doi: 10.1097/00001756-199905140-00012. PubMed DOI
Rilling JK, Glasser MF, Preuss TM, Ma X, Zhao T, Hu X, Behrens TEJ. The evolution of the arcuate fasciculus revealed with comparative DTI. Nature Neuroscience. 2008;11:426–428. doi: 10.1038/nn2072. PubMed DOI
Ringo JL, Doty RW, Demeter S, Simard PY. Time is of the essence: a conjecture that hemispheric specialization arises from interhemispheric conduction delay. Cerebral Cortex. 1994;4:331–343. doi: 10.1093/cercor/4.4.331. PubMed DOI
Rogers LJ. Hand and paw preferences in relation to the lateralized brain. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 2009;364:943–954. doi: 10.1098/rstb.2008.0225. PubMed DOI PMC
Roos C, Liedigk R, Thinh VN, Nadler T, Zinner D. The hybrid origin of the Indochinese gray langur Trachypithecus crepusculus. International Journal of Primatology. 2019;40:9–27. doi: 10.1007/s10764-017-0008-4. DOI
Sanford C, Guin K, Ward JP. Posture and laterality in the bushbaby (Galago senegalensis) Brain, Behavior and Evolution. 1984;25:217–224. doi: 10.1159/000118867. PubMed DOI
Schmitt V, Melchisedech S, Hammerschmidt K, Fischer J. Hand preferences in barbary macaques (Macaca sylvanus) Laterality. 2008;13:143–157. doi: 10.1080/13576500701757532. PubMed DOI
Schmitz J, Lor S, Klose R, Güntürkün O, Ocklenburg S. The functional genetics of handedness and language lateralization: insights from gene ontology, pathway and disease association analyses. Frontiers in Psychology. 2017a;8:1144. doi: 10.3389/fpsyg.2017.01144. PubMed DOI PMC
Schmitz J, Metz GAS, Güntürkün O, Ocklenburg S. Beyond the genome-towards an epigenetic understanding of handedness ontogenesis. Progress in Neurobiology. 2017b;159:69–89. doi: 10.1016/j.pneurobio.2017.10.005. PubMed DOI
Schweitzer C, Bec P, Blois-Heulin C. Does the complexity of the task influence manual laterality in de brazza’s monkeys (Cercopithecus neglectus)? Ethology. 2007;113:983–994. doi: 10.1111/j.1439-0310.2007.01405.x. DOI
Sha Z, Pepe A, Schijven D, Carrión-Castillo A, Roe JM, Westerhausen R, Joliot M, Fisher SE, Crivello F, Francks C. Handedness and its genetic influences are associated with structural asymmetries of the cerebral cortex in 31,864 individuals. PNAS. 2021;118:e2113095118. doi: 10.1073/pnas.2113095118. PubMed DOI PMC
Silcox MT, Bloch JI, Boyer DM, Godinot M, Ryan TM, Spoor F, Walker A. Semicircular canal system in early primates. Journal of Human Evolution. 2009;56:315–327. doi: 10.1016/j.jhevol.2008.10.007. PubMed DOI
Spoelstra K. Lateralized Behavior in White-Handed Gibbons: Hylobates lar. Master Thesis. Linköping University, Linköping; 2021.
Sussman RW, Tab Rasmussen D, Raven PH. Rethinking primate origins again. American Journal of Primatology. 2013;75:95–106. doi: 10.1002/ajp.22096. PubMed DOI
Tan Y, Yoder AD, Yamashita N, Li WH. Evidence from opsin genes rejects nocturnality in ancestral primates. PNAS. 2005;102:14712–14716. doi: 10.1073/pnas.0507042102. PubMed DOI PMC
Toth N. Archaeological evidence for preferential right-handedness in the lower and middle Pleistocene, and its possible implications. Journal of Human Evolution. 1985;14:607–614. doi: 10.1016/S0047-2484(85)80087-7. DOI
Vauclair J, Meguerditchian A, Hopkins WD. Hand preferences for unimanual and coordinated bimanual tasks in baboons (Papio anubis) Brain Research. Cognitive Brain Research. 2005;25:210–216. doi: 10.1016/j.cogbrainres.2005.05.012. PubMed DOI PMC
Ward JP. Left hand advantage for prey capture in the galago (Galago moholi) International Journal of Comparative Psychology. 1998;11:173–184.
Westergaard GC, Suomi SJ. Hand preference for a bimanual task in tufted capuchins (Cebus apella) and rhesus macaques (Macaca mulatta) Journal of Comparative Psychology. 1996;110:406–411. doi: 10.1037/0735-7036.110.4.406. PubMed DOI
Westergaard GC, Kuhn HE, Suomi SJ. Bipedal posture and hand preference in humans and other primates. Journal of Comparative Psychology. 1998;112:55–64. doi: 10.1037/0735-7036.112.1.55. PubMed DOI
Yousry TA, Schmid UD, Alkadhi H, Schmidt D, Peraud A, Buettner A, Winkler P. Localization of the motor hand area to a knob on the precentral gyrus: A new landmark. Brain. 1997;120 (Pt 1):141–157. doi: 10.1093/brain/120.1.141. PubMed DOI
Zhao D, Hopkins WD, Li B. Handedness in nature: first evidence on manual laterality on bimanual coordinated tube task in wild primates. American Journal of Physical Anthropology. 2012;148:36–44. doi: 10.1002/ajpa.22038. PubMed DOI PMC
Dryad
10.5061/dryad.8sf7m0crv