A comparative assessment of handedness and its potential neuroanatomical correlates in chimpanzees (Pan troglodytes) and bonobos (Pan paniscus)

in Behaviour
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The evolutionary origins of human right-handedness remain poorly understood. Some have hypothesized that tool use served as an important preadaptation for the eventual evolution of population-level right-handedness. In contrast, others have suggested that complex gestural and vocal communication served as prerequisite for the evolution of human right-handedness. In this study, we tested these competing hypotheses by comparing the handedness of bonobos and chimpanzees, two closely related species of Pan, on three different measures of hand use including simple reaching, manual gestures and coordinated bimanual actions. Chimpanzees are well known for their tool using abilities whereas bonobos rarely use tools in the wild. In contrast, many have suggested that bonobos have a more flexible gestural and vocal communication system than chimpanzees. The overall results showed that chimpanzees were significantly more right-handed than bonobos for all three measures suggesting that adaptations for tool use rather than communication may have led to the emergence of human right-handedness. We further show that species differences in handedness may be linked to variation in the size and asymmetry of the motor-hand area of the precentral gyrus. The results are discussed within the context of evolutionary theories of handedness, as well as some limitations in the approach to handedness measurement in nonhuman primates.

A comparative assessment of handedness and its potential neuroanatomical correlates in chimpanzees (Pan troglodytes) and bonobos (Pan paniscus)

in Behaviour

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References

AlkadhiH.KolliasS.S. (2004). Pli de passage fronto-parietal moyen of Broca separates the motor homoculus. — Am. J. Neuroradiol. 25: 809-812.

AnnettM. (2002). Handedness and brain asymmetry: the right shift theory. — Psychology PressHove.

BaileyP.von BoninG.McCullochW.S. (1950). The isocortex of the chimpanzee. — University of Illinois PressUrbana-Champaign, IL.

BiroD.Inoue-NakamuraN.TonookaR.YamakoshiG.SousaC.MatsuzawaT. (2003). Cultural innovation and transmission of tool use in wild chimpanzees: evidence from field experiments. — Anim. Cogn. 6: 213-223.

BiroD.SousaC.MatsuzawaT. (2006). Ontogeny and cultural propagation of tool use by wild chimpanzees at Bossou, Guinea: case studies in nut cracking and leaf folding. — In: Cognitive development of chimpanzees ( MatsuzawaT.TomonagaT.TanakaM. eds). SpringerNew York, NY p.  476-507.

BoeschC. (1991). Handedness in wild chimpanzees. — Int. J. Primatol. 6: 541-558.

BogartS.L.ManginJ.-F.SchapiroS.J.ReamerL.BennettA.J.PierreP.J.HopkinsW.D. (2012a). Cortical sulci asymmetries in chimpanzees and macaques: a new look at an old idea. — NeuroImage 61: 533-541.

BogartS.L.PruetzJ.D.OrmistonL.K.RussellJ.L.MeguerditchianA.HopkinsW.D. (2012b). Termite fishing laterality in the Fongoli savanna chimpanzees (Pan troglodytes verus): further evidence of a left hand preference. — Am. J. Phys. Anthropol. 149: 591-598.

BogartS.L.BennettA.J.SchapiroS.J.ReamerL.A.HopkinsW.D. (2014). Different early rearing experiences have long term effects on cortical organziation in captive chimpanzees (Pan troglodytes). — Dev. Sci. 17: 161-174.

BolingW.OlivierA.BittarR.ReutensD. (1999). Localization of hand motor activation in Broca’s pli de passage moyen. — J. Neurosurg. 91: 903-910.

BoysenS.T.KuhlmeierK.HallidayP.HallidayY.M. (1999). Tool use in captive gorillas. — In: The mentality of gorillas and orangutans ( ParkerS.T.MitchellR.W.MilesH.L. eds). Cambridge University PressCambridge.

BradshawB.RogersL. (1993). The evolution of lateral asymmetries language tool-use and intellect. — Academic PressSan Diego, CA.

BradshawJ.L. (1997). Human evolution: a neuropsychological perspective. — Psychology PressHove.

BrakkeK.E.Savage-RumbaughE.S. (1995). The development of language skills in bonobo and chimpanzee — I. Comprehension. — Lang. Commun. 15: 121-148.

BrakkeK.E.Savage-RumbaughE.S. (1996). The development of language skills in Pan — II. Production. — Lang. Commun. 16: 361-380.

ButterworthG.ItakuraS. (1998). Development of precision grips in chimpanzees. — Dev. Sci. 1: 39-43.

ByrneR.W.ByrneJ.M. (1991). Hand preferences in the skilled gathering tasks of mountain gorillas (Gorilla gorilla berengei). — Cortex 27: 521-536.

CashmoreL. (2009). Can hominin “handedness” be accuartely assessed?Ann. Hum. Biol. 36: 624-641.

CashmoreL.UominiN.ChapelainA. (2008). The evolution of handedness in humans and great apes: a review and current issues. — J. Anthropol. Sci. 86: 7-35.

ChapelainA.HogervorstE. (2009). Hand preferences for bimanual coordination in 29 bonobos (Pan paniscus). — Behav. Brain Res. 196: 15-29.

ChapelainA.HogervorstE.MbonzoP.HopkinsW.D. (2011). Hand preferences for bimanual coordination in 77 bonobos (Pan paniscus): replication and extension. — Int. J. Primatol. 32: 491-510.

ChristelM.I.KitzelS.NiemitzC. (1998). How precisely do bonobos (Pan paniscus) grasp small objects?Int. J. Primatol. 19: 165-194.

ClayZ.ZuberbuhlerK. (2011). Bonobos extract meaning from call sequences. — PLoS One 6: e18786.

CorballisM.C. (1992). The lopsided brain: Evolution of the generative mind. — Oxford University PressNew York, NY.

CorballisM.C. (2002). From hand to mouth: the origins of language. — Princeton University PressPrinceton, NJ.

CoulonO.ClouchouxC.OperatoG.DauchotK.SiriguA.AntonJ.-L. (2006). Cortical localization via surface parameterization: a sulcus-based approach. — NeuroImage 31: S46.

CykowskiM.D.CoulonO.KochunovP.V.AmuntsK.LancasterJ.L.LairdA.R.GlahnC.FoxP.T. (2008). The central sulcus: an observer-independent characterization of sulcal landmarks and depth asymmetry. — Cerebr. Cort. 18: 1999-2009.

DaddaM.CantalupoC.HopkinsW.D. (2006). Further evidence of an association between handedness and neuroanatomical asymmetries in the primary cortex of chimpanzees (Pan troglodytes). — Neuropsychologia 44: 2482-2486.

DavatzikosC.BryanR.N. (2002). Morphometric analysis of cortical sulci using parametric ribbons: a study of the central sulcus. — J. Comput. Assis. Tomogr. 26: 298-307.

de WaalF.B.M. (1989). Behavioral contrasts between bonobo and chimpanzee. — In: Understanding chimpanzees ( HeltneP.G.MarquardtL.A. eds). Harvard University PressCambridge, MA p.  154-175.

FischerA.WiebeV.PääboS.PrzeworskiM. (2004). Evidence for a complex demographic history of chimpanzees. — Mol. Biol. Evol. 21: 799-808.

ForresterG.S.LeavensD.A.QuaresminiC.VallortigaraG. (2011). Target animacy influences gorilla handedness. — Anim. Cogn. 14: 903-907.

ForresterG.S.QuaresminiC.LeavensD.A.SpiezioC.VallortigaraG. (2012). Target animacy influences chimpanzee handedness. — Anim. Cogn. 15: 1121-1127.

FrostG.T. (1980). Tool behavior and the origin of laterality. — J. Hum. Evol. 9: 447-459.

GallupG.G. (1970). Chimpanzees: self-recognition. — Science 167: 86-87.

GibsonK.R.IngoldT. (1993). Tools language and cognition in human evolution. — Cambridge University PressCambridge.

GreenfieldP.M. (1991). Language, tools, and brain: the ontogeny and phylogeny of hierarchically organized sequential behavior. — Behav. Brain Sci. 14: 531-550.

GreenfieldP.M.Savage-RumbaughE.S. (1990). Grammatical combination in Pan paniscus: processes of learning and invention in the evolution and development of language. — In: “Language” and intelligence in monkeys and apes: comparative developmental perspectives ( ParkerS.T.GibsonK.R. eds). Cambridge University PressNew York, NY p.  540-578.

GruberT.ClayZ.ZuberbuhlerK. (2010). A comparison of bonobo and chimpanzee tool use: evidence for a femle bias in the Pan lineage. — Anim. Behav. 80: 1023-1033.

HammondG. (2002). Correlates of human handedness in primary motor cortex: a review and hypothesis. — Neurosci. Biobehav. Rev. 26: 285-292.

HareB. (2007). From nonhuman to human mind. what changed and why?Curr. Direct. Psychol. Sci. 16: 60-64.

HareB.TomaselloM. (2004). Chimpanzees are more skillful in competitive than in cooperative cognitive tasks. — Anim. Behav. 68: 571-581.

HareB.MelisA.P.WoodsV.HastingsS.WranghamR. (2007). Tolerance allows bonobos to outperform chimpanzees on a cooperative task. — Curr. Biol. 17: 619-623.

HarrisonR.M.NystromP. (2008). Handedness in captive bonobos (Pan paniscus). — Folia Primatologica 79: 253-268.

Herculano-HouzelS.MotaB.WongP.KaasJ.H. (2010). Connectivity-driven white matter scaling and folding in primate cerebral cortex. — Proc. Natl. Acad. Sci. USA 107: 19008-19013.

HerrmannE.HareB.CallJ.TomaselloM. (2010). Differences in the cognitive skills of bonobos and chimpanzees. — PLoS One 5: e12438.

HopkinsW.D. (1995a). Hand preferences for a coordinated bimanual task in 110 chimpanzees: cross-sectional analysis. — J. Comp. Psychol. 109: 291-297.

HopkinsW.D. (1995b). Hand preferences in juvenile chimpanzees: continuity in development. — Dev. Psychol. 31: 619-625.

HopkinsW.D. (2007). Hemispheric specialization in chimpanzees: evolution of hand and brain. — In: Evolutionary cognitive neuroscience ( ShackelfordT.KeenanJ.P.PlatekS.M. eds). MIT PressCambridge, MA p.  99-120.

HopkinsW.D.CantalupoC. (2004). Handedness in chimpanzees is associated with asymmetries in the primary motor but not with homologous language areas. — Behav. Neurosci. 118: 1176-1183.

HopkinsW.D.de WaalF.B.M. (1995). Behavioral laterality in captive bonobos (Pan paniscus): replication and extension. — Int. J. Primatol. 16: 261-276.

HopkinsW.D.PilcherD.L. (2001). Neuroanatomical localization of the motor hand area with magnetic resonance imaging: the left hemisphere is larger in Great Apes. — Behav. Neurosci. 115: 1159-1164.

HopkinsW.D.RussellJ.L. (2004). Further evidence of a right hand advantage in motor skill by chimpanzees (Pan troglodytes). — Neuropsychologia 42: 990-996.

HopkinsW.D.Savage-RumbaughE.S. (1991). Vocal communication as a function of differential rearing experiences in Pan paniscus: a preliminary report. — Int. J. Primatol. 12: 559-583.

HopkinsW.D.CantalupoC.WesleyM.J.HostetterA.B.PilcherD. (2002). Grip morphology and hand use in chimpanzees (Pan troglodytes): evidence of a left hemisphere specialization in motor skill. — J. Exp. Psychol. 131: 412-423.

HopkinsW.D.WesleyM.J.IzardM.K.HookM.SchapiroS.J. (2004). Chimpanzees are predominantly right-handed: replication in three colonies of apes. — Behav. Neurosci. 118: 659-663.

HopkinsW.D.RussellJ.FreemanH.BuehlerN.ReynoldsE.SchapiroS. (2005a). The distribution and development of handedness for manual gestures in captive chimpanzees (Pan troglodytes). — Psych. Sci. 16: 487.

HopkinsW.D.RussellJ.HookM.BracciniS.SchapiroS. (2005b). Simple reaching is not so simple: association between hand use and grip preferences in captive chimpanzees. — Int. J. Primatol. 26: 259-277.

HopkinsW.D.RussellJ.L.FreemanH.BuehlerN.ReynoldsE.SchapiroS.J. (2005c). The distribution and development of handedness for manual gestures in captive chimpanzees (Pan troglodytes). — Psychol. Sci. 16: 487-493.

HopkinsW.D.RussellJ.L.HookM.BracciniS.SchapiroS.J. (2005d). Simple reaching is not so simple: association between hand use and grip preferences in captive chimpanzees. — Int. J. Primatol. 26: 259-277.

HopkinsW.D.RussellJ.L.CantalupoC. (2007). Neuroanatomical correlates of handedness for tool use in chimpanzees (Pan troglodytes): implication for theories on the evolution of language. — Psychol. Sci. 18: 971-977.

HopkinsW.D.LynH.CantalupoC. (2009). Volumetric and lateralized differences in selected brain regions of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus). — Am. J. Primatol. 71: 988-997.

HopkinsW.D.CoulonO.ManginJ.F. (2010). Observer-independent characterization of sulcal landmarks and depth asymmetry in the central sulcus of the chimpanzee brain. — Neuroscience 171: 544-551.

HopkinsW.D.PhillipsK.A.BaniaA.CalcuttS.E.GardnerM.RussellJ.L.SchaefferJ.A.von LonsdorfE.RossS.SchapiroS.J. (2011). Hand preferences for coordinated bimanual actions in 777 great apes: implications for the evolution of handedness in Hominins. — J. Hum. Evol. 60: 605-611.

HopkinsW.D.PikaS.LiebalK.BaniaA.MeguerditchianA.GardnerM.SchapiroS.J. (2012). Handedness for manual gestures in great apes: a meta-analysis. — In: Current developments in non-human primate gesture research ( PikaS.LiebalK. eds). John Benjamins PublishingAmsterdam.

HumleT.MatsuzawaT. (2009). Laterality in hand use across four tool use behaviors among the wild chimpanzees of Bossou, Guinea, West Africa. — Am. J. Primatol. 71: 40-48.

HyattC.W.HopkinsW.D. (1994). Self-awareness in bonobos and chimpanzees: a comparative perspective. — In: Self-awareness in animals and humans: developmental perspectives ( ParkerS.T.MitchellR.W.BocciaM.L. eds). Cambridge University PressNew York, NY p.  248-253.

Jones-EngelL.E.BardK.A. (1996). Precision grips in young chimpanzees. — Am. J. Primatol. 39: 1-15.

LambertM. (2012). Hand preference for bimanual and unimanual feeding in captive gorillas: extension in a second colony of apes. — Am. J. Phys. Anthropol. 148: 641-647.

LeavensD.A.HopkinsW.D. (1998). Intentional communication by chimpanzee (Pan troglodytes): a cross-sectional study of the use of referential gestures. — Dev. Psychol. 34: 813-822.

LilakA.L.PhillipsK.A. (2007). Consistency in hand preference across low-level and high-level tasks in capuchin monkeys (Cebus apella). — Am. J. Primatol. 69: 1-12.

LlorenteM.PalouL.CarrascoL.RibaD.MosqueraM.ColellM.FabreM.FeliuO. (2010). Population-level right handedness for a coordinated bimanual task in naturalistic housed chimpanzees: replication and extension in 114 animals from Zambia and Spain. — Am. J. Primatol. 71: 1-10.

LynH. (2007). Mental representation of symbols as revealed by vocabulary errors in two bonobos (Pan paniscus). — Anim. Cogn. 10: 461-475.

LynH.GreenfieldP.M.Savage-RumbaughE.S. (2006). The development of representational play in chimpanzees and bonobos: evolutionary implications, pretense, and the role of interspecies communication. — Cogn. Dev. 21: 199-213.

LynH.GreenfieldP.M.Savage-RumbaughE.S. (2011). Semiotic combinations in Pan: a cross-species comparison of communication in a chimpanzee and a bonobo. — First Lang. 31: 300-325.

ManginJ.F.RiviereD.CachiaA.DuchesnayE.CointepasY.Papadopoulos-OrfanosD.CollinsD.L.EvansA.C.RegisJ. (2004). Object-based morphometry of the cerebral cortex. — Med. Imag. 23: 968-982.

MarchantL.F.McGrewW.C. (2007). Ant fishing by wild chimpanzees is not lateralised. — Primates 48: 22-26.

McGrewW.C. (1992). Chimpanzee material culture: implications for human evolution. — Cambridge University PressCambridge.

McGrewW.C.MarchantL.F. (1992). Chimpanzees, tools, and termites: hand preference or handedness?Curr. Anthropol. 33: 114-119.

McGrewW.C.MarchantL.F. (1993). Are gorillas right-handed or not?Hum. Evol. 8: 17-23.

McGrewW.C.MarchantL.F. (1996). On which side of the apes? — In: Great ape societies ( McGrewW.C.MarchantL.F.NishidaT. eds). Cambridge University PressCambridge p.  255-272.

McGrewW.C.MarchantL.F. (1997). Using the tools at hand: manual laterality and elementary technology in Cebus spp. and Pan spp.Int. J. Primatol. 18: 787-810.

MeguerditchianA.CalcuttS.E.von LonsdorfE.RossS.R.HopkinsW.D. (2010a). Captive gorillas are right-handed for bimanual feeding. — Am. J. Phys. Anthropol. 141: 638-645.

MeguerditchianA.VauclairJ.HopkinsW.D. (2010b). Captive chimpanzees use their right hand to communicate with each other: implications for the origins of hemispheric specialization for language. — Cortex 46: 40-48.

MeunierH.VauclairJ. (2007). Hand preferences on unimanual and bimanual tasks in white-face capuchins. — Am. J. Primatol. 69: 1064-1069.

ParishA.R. (1996). Female relationships in bonobos (Pan paniscus) — evidence for bonding, cooperation, and female dominance in a male-philopatric species. — Hum. Nat. Interdisc. Biosoc. Perspect. 7: 61-96.

ParishA.R.de WaalF.B.M.HaigD. (2000). The other “closest living relative”: how bonobos (Pan paniscus) challenge traditional assumptions about females, dominance, intra- and intersexual interactions, and hominid evolution. — Ann. NY Acad. Sci. 907: 97-113.

ParkerS.KerrM.MarkowitzH.GouldJ. (1999). A survey of tool use in zoo gorillas. — In: The mentalities of gorillas and orangutans: comparative perspectives ( ParkerS.T.MitchellR.W. eds). Cambridge University PressCambridge.

PhillipsK.A.SherwoodC.C. (2005). Primary motor cortex asymmetry is correlated with handedness in capuchin monkeys (Cebus apella). — Behav. Neurosci. 119: 1701-1704.

PikaS.LiebalK.TomaselloM. (2005). The gestural repertoire of bonobos (Pan paniscus): flexibility and use. — Am. J. Primatol. 65: 39-61.

PollickA.S.de WaalF.B.M. (2007). Ape gestures and language evolution. — Proc. Natl. Acad. Sci. USA 104: 8184-8189.

RillingJ.K.ScholzJ.PreussT.M.GlasserM.F.ErrangiB.V.BehrensT.E.J. (2012). Differences between chimpanzees and bonobos in neural systems supporting social cognition. — Soc. Cogn. Affect. Neurosci. 7: 369-379.

RosatiA.G.HareB. (2012). Chimpanzees and bonobos exhibit divergent spatial memory development. — Dev. Sci. 15: 840-853.

Savage-RumbaughE.S. (1984). Pan paniscus and Pan troglodytes: contrast in preverbal communicative competence. — In: The pygmy chimpanzee: evolutionary biology and behavior ( SusmanR.L. ed.). Plenum PressNew York, NY p.  395-413.

ShaferD.D. (1997). Hand preference behaviors shared by two groups of captive bonobos. — Primates 38: 303-313.

SpinozziG.CastorninaM.G.TruppaV. (1998). Hand preferences for unimanual and coordinated-bimanual tasks in tufted capuchin monkeys (Cebus apella). — J. Comp. Psychol. 112: 183-191.

StanfordC.B. (1998). The social behavior of chimpanzees and bonobos: empirical evidence and shifting assumptions. — Curr. Anthropol. 39: 399-420.

TablowoE.ForresterG.S. (2013). Stuctured bimanual actions and hand transfers reveal population-level right handedness in captive gorillas. — Anim. Behav. 86: 1049-1057.

TaglialatelaJ.P.Savage-RumbaughE.S.BakerL.A. (2003). Vocal production by a language-competent Pan paniscus. — Int. J. Primatol. 24: 1-17.

TonookaR.MatsuzawaT. (1995). Hand preferences in captive chimpanzees (Pan troglodytes) in simple reaching for food. — Int. J. Primatol. 16: 17-34.

TothN.SchickK.D.Savage-RumbaughE.S.SevcikR.A.RumbaughD.M. (1993). Pan the tool-maker: investigations into the stone tool-making and tool-using capabilities of a bonobo (Pan paniscus). — J. Archaeol. Sci. 20: 81-91.

UominiN.T. (2009). The prehistory of handedness: archeological data and comparative ethology. — J. Hum. Evol. 57: 411-419.

van EssenD.C. (1997). A tension-based theory of morphogenesis and compact wiring in the central nervous system. — Nature 385: 313-318.

von LonsdorfE.HopkinsW.D. (2005). Wild chimpanzees show population level handedness for tool use. — Proc. Natl. Acad. Sci. USA 102: 12634-12638.

WestergaardG.C.LussierI.D.HigleyJ.D. (2001). Between-species variation in the development of hand preference among macaques. — Neuropsychologia 39: 1373-1378.

WhitenA.GoodallJ.McGrewW.NishidaT.ReynoldsV.SugiyamaY.TutinC.WranghamR.BoeschC. (2001). Charting cultural variation in chimpanzees. — Behaviour 138: 1489-1525.

WhitenA.GoodallJ.McGrewW.C.NishidaT.ReynoldsV.SugiyamaY.TutinC.E.G.WranghamR.W.BoeschC. (1999). Cultures in chimpanzees. — Nature 399: 682-685.

WonY.-J.HeyJ. (2005). Divergence population genetics of chimpanzees. — Mol. Biol. Evol. 22: 297-307.

YousryT.A.SchmidU.D.AlkadhiH.SchmidtD.PeraudA.BuettnerA.WinklerP. (1997). Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. — Brain 120: 141-157.

Figures

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    BrainVISA’s pipeline processing steps. (a) MR image of a skull-stripped chimpanzee brain, (b) stable tissue intensities after bias field correction, (c) binary mask of the brain, (d) split mask of left and right hemispheres and cerebellum, (e) grey and white interface, (f) negative mould of the white matter, (g) skeletonised mould of cortical folding and (h) cortical fold graph of chimpanzee sulci with the central sulcus in red. This figure is published in colour in the online edition of this journal, which can be accessed via http://booksandjournals.brillonline.com/content/journals/1568539x.

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    3-D reconstruction of cortical sulci of the chimpanzee and bonobo brain with the central sulcus (red) indicated in each species. This figure is published in colour in the online edition of this journal, which can be accessed via http://booksandjournals.brillonline.com/content/journals/1568539x.

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    Chimpanzee central sulcus labeled and extracted. (a) The surface area and depth dimensions are shown in the extracted sulcus, as well as the x- and y-coordinates used for computing differences in cortical folding of the CS along the dorsal–ventral axis. (b) Illustration of the landmarks used to quantify grey matter thickness. This figure is published in colour in the online edition of this journal, which can be accessed via http://booksandjournals.brillonline.com/content/journals/1568539x.

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    (a) Chimpanzee central sulcus and (b, c) the surface area and depth dimensions are shown in the extracted sulcus, as well as the x- and y-coordinates used for computing differences in cortical folding of the CS along the dorsal–ventral axis (d) outputted data from CS parameterization. Depth of CS is plotted on ordinate and the y coordinate along the abscissa. SP, superior maximum; CS, depth before y coordinate 50; IP, maximum inferior depth after y coordinate 50; PPFM, pli-de-passage moyen parietale, which is the shallowest CS depth measure between the SP and IP y coordinates. This figure is published in colour in the online edition of this journal, which can be accessed via http://booksandjournals.brillonline.com/content/journals/1568539x.

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    Variation in CS depth along the Superior-Inferior plane in the chimpanzee (purple line) and bonobos (blue line). SP, maximum superior depth; PPFM, shallowest CS depth point between SP and IP; IP, maximum inferior depth. This figure is published in colour in the online edition of this journal, which can be accessed via http://booksandjournals.brillonline.com/content/journals/1568539x.

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    Mean HI scores (±SE) for each handedness task (gesture, TUBE, and reach) and the overall score in bonobos and chimpanzees.

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    Mean HI scores (±SE) in manual gestures from previous studies compared to the data reported in this study.

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