the evolution of human and ape hand proportions · the evolution of human and ape hand proportions...

ARTICLEReceived 6 Feb 2015 | Accepted 4 Jun 2015 | Published 14 Jul 2015

The evolution of human and ape hand proportionsSergio Almecija123 Jeroen B Smaers4 amp William L Jungers2

Human hands are distinguished from apes by possessing longer thumbs relative to fingers

However this simple ape-human dichotomy fails to provide an adequate framework for

testing competing hypotheses of human evolution and for reconstructing the morphology of

the last common ancestor (LCA) of humans and chimpanzees We inspect human and

ape hand-length proportions using phylogenetically informed morphometric analyses and

test alternative models of evolution along the anthropoid tree of life including fossils like

the plesiomorphic ape Proconsul heseloni and the hominins Ardipithecus ramidus and

Australopithecus sediba Our results reveal high levels of hand disparity among modern

hominoids which are explained by different evolutionary processes autapomorphic evolution

in hylobatids (extreme digital and thumb elongation) convergent adaptation between

chimpanzees and orangutans (digital elongation) and comparatively little change in gorillas

and hominins The human (and australopith) high thumb-to-digits ratio required little change

since the LCA and was acquired convergently with other highly dexterous anthropoids

DOI 101038ncomms8717 OPEN

1 Center for the Advanced Study of Human Paleobiology Department of Anthropology The George Washington University Washington DC 20052 USA2 Department of Anatomical Sciences Stony Brook University Stony Brook New York 11794 USA 3 Institut Catala de Paleontologia Miquel Crusafont (ICP)Universitat Autonoma de Barcelona Edifici Z (ICTA-ICP) campus de la UAB c de les Columnes sn 08193 Cerdanyola del Valles (Barcelona) Spain4 Department of Anthropology Stony Brook University Stony Brook New York 11794 USA Correspondence and requests for materials should be addressedto SA (email sergioalmecijagmailcom)

NATURE COMMUNICATIONS | 67717 | DOI 101038ncomms8717 | wwwnaturecomnaturecommunications 1

amp 2015 Macmillan Publishers Limited All rights reserved

The hand is one of the most distinctive traits of humankindand one of our main sources of interaction with theenvironment1 The human hand can be distinguished

from that of apes by its long thumb relative to fingers1ndash4 (Fig 1a)which has been related functionally to different selectiveregimesmdashmanipulation vs locomotionmdashacting on human andape hands15 During the first half of the twentieth centurytheories on human evolution were dominated by the view thathumans split very early from the common stock of apes andlargely preserved generalized (plesiomorphic) hand proportionssimilar to other anthropoid primates6ndash8 To the contrary extantapes were seen as extremely specialized animals adapted forbelow-branch suspension67 However since the molecularrevolution in the 1980ndash1990s (which provided unequivocalevidence for humans and chimpanzees being sister taxa)9 aprevalent and influential evolutionary paradigmmdashsaid to be basedon parsimonymdashhas assumed that the last common ancestor(LCA) of chimpanzees and humans was similar to a modernchimpanzee (for example ref 10) This shift resurrected thelsquotroglodytianrsquo stage in human evolution which assumes that achimp-like knuckle-walking ancestor preceded human bipedalism(for example ref 11) Most subsequent hypotheses dealing withhuman hand evolution have been framed assuming a lsquolong-handedshort-thumbedrsquo chimp-like hand as the starting points ofthe LCA and basal hominins with strong selective pressuresacting to reverse these proportions in the context of stone tool-making andor as a by-product of drastic changes in footmorphology in the human career (for example ref 12) Howeverthe current fossil evidence of early hominins251314 and fossil

apes15ndash18 challenges this paradigm Collectively these fossilssuggest instead that hand proportions approaching the modernhuman condition could in fact be largely plesiomorphic2413 aswas previously suggested before the advent of molecularphylogenetics If that were the case this would have profoundimplications relevant to the locomotor adaptations of thechimpanzee-human LCA as well as the relationship betweenhuman hand structure and the origins of systematized stone toolculture

To address this complex discussion and to provide a deeperunderstanding on the evolution of the human and ape hand inthis study we perform a stepwise series of detailed morphometricand evolutionary analyses on the hand-length proportions ofmodern apes and humans as compared with a large sample ofextant anthropoid primates and key fossils preserving sufficientlycomplete associated hands This fossil sample is constituted bythe early hominins Ardipithecus ramidus (44 Myr ago)2 andAustralopithecus sediba (B2 Myr ago)14 as well as the primitiveAfrican ape Proconsul heseloni (B18 Myr ago)15 and the Europeanfossil great ape Hispanopithecus laietanus (96 Myr ago)17 First weinspect thumb length relative to the lateral digits (as revealed byray four that is intrinsic hand proportions) to show thathumans are distinctive from apes for this important functionalmeasure but not from some other anthropoids Second weanalyse individual hand elements as proportions adjusted viaoverall body size (that is extrinsic hand proportions) to testwhether modern apesmdashand more especially African greatapesmdashrepresent a homogeneous group from which humansdepart Here we further show that modern hominoids constitute

AlouattaCebus

NasalisMacaca

MandrillusPapio

TheropithecusHylobatidae

Po pygmaeusPo abeliiG gorilla

G beringeiPa paniscus

Pa troglodytesHo sapiens

ARA-VP-6500Ar ramidus

Pr heseloniKebara 2

Ho neanderthalensis

MH2Au sediba

Qafzeh 9early Ho sapiens

Relative thumb length (intrinsic)085075065055045035

Chimpanzee Human

a b Modern humansModern apes

Figure 1 | Intrinsic hand proportions of humans and other anthropoid primates (a) Drawings of a chimpanzee and human hands are shown to similarscale (b) Relative length of the thumbfrac14 pollicalfourth ray lengths (minus distal fourth phalanx see inset) Box represents the interquartile rangecenterline is the median whiskers represent non-outlier range and dots are outliers The ranges of humans and modern apes are highlighted (green andred-shaded areas respectively) Samples for each boxplot are Homo sapiens (nfrac1440) Pan troglodytes (nfrac14 34) Pan paniscus (nfrac14 12) Gorilla beringei (nfrac14 21)Gorilla gorilla (nfrac14 13) Pongo abelii (nfrac148) Pongo pygmaeus (nfrac14 19) Hylobatidae (nfrac14 14) Theropithecus (nfrac14 5) Papio (nfrac14 50) Mandrillus (nfrac14 3) Macaca(nfrac14 18) Nasalis (nfrac14 14) Cebus (nfrac14 11) and Alouatta (nfrac14 8) The values for Pr heseloni and Ar ramidus are projected onto the remaining taxa to facilitatevisual comparisons

ARTICLE NATURE COMMUNICATIONS | DOI 101038ncomms8717

2 NATURE COMMUNICATIONS | 67717 | DOI 101038ncomms8717 | wwwnaturecomnaturecommunications


a highly heterogeneous group with differences that cannot beexplained by phylogenetic proximity or size-related effectsThird we enlist phylogenetically informed comparative methodsto map how the evolution of hand-length proportions has playedout along the individual lineages of our comparative sampleThese methods employ statistical models that establish principlesof how continuous trait change is likely to have unfoldedover time and we explore those principles to infer how thevariation observed in comparative trait measurements is likely tohave changed along the individual branches of a (independentlyderived molecular-based) phylogeny Importantly from astatistical viewpoint these methods allow the comparative data(including the fossils) to be analysed within an alternative-hypothesis-testing framework that assesses the statistical fit ofalternative evolutionary scenarios In our case we determine howhand-length proportions changed over time and quantify therelative likelihood support of alternative evolutionary hypothesisthus providing a novel and rigorous analysis of human and apehand evolution

Our results reveal that the different hand morphologiesexhibited by modern hominoids reflect different evolutionaryprocesses hylobatids display an autapomorphic hand due toextreme digital and thumb elongation chimpanzees and orangu-tans exhibit convergent adaptation related to digital elongation (toa lesser degree than hylobatids) whereas the gorilla and homininlineages experienced little change by comparison (that is theiroverall hand proportions are largely plesiomorphic withincatarrhines) These results support the view that the long thumbrelative to fingers characterizing the human (and australopith)hand required little change since the chimpanzee-human LCAand was acquired in convergence with other highly dexterousanthropoids such as capuchins and gelada baboons

ResultsIntrinsic hand proportions Hand proportions of humans areusually compared with those of apes using the thumb-to-digitratio (or IHPs) which is a good functional measure of thumbopposability and therefore a proxy for manual dexterity (forexample refs 11419) Accordingly we queried our anthropoidsample (see details of our sample in Supplementary Table 1) tosee whether our IHP measure (as revealed by the thumb-to-

fourth ray ratio Fig 1b) was consistent with previous observa-tions that humans can easily be distinguished from modern apesby a long thumb relative to the other digits4514 The modernhuman IHP range is well above that of modern apes (that is nooverlap analysis of variance (ANOVA) with Bonferroni post hoccomparisons Po0001 see Supplementary Table 2 for details onthe taxa-specific comparisons) which can be linked directly tothe human capability (unique among modern hominoids20) toperform an efficient lsquopad-to-pad precision graspingrsquo (that isbroad contact of the distal pads of the thumb and index fingerSupplementary Note 1)14513 In contrast chimpanzees andespecially orangutans are found to have significantly shorterthumbs than gorillas and hylobatids (ANOVA with Bonferronipost hoc comparisons Po0001) Fossil hominins fall withinthe modern human range but Ar ramidus exhibits a shorterthumb (within the gorilla-hylobatid range) implying limitsto its precision grasping capabilities Most non-hominoidanthropoids including the fossil ape Pr heseloni exhibit IHPranges in-between modern apes and humans Both Cebus andTheropithecus overlap in this index with humans supporting therelationship between this ratio and enhanced manipulative skills(see Supplementary Note 1)

Extrinsic hand proportions Despite the aforementioned func-tional connections IHPs provide limited information regardingwhat distinguishes humans from apes is it a longer thumbshorter digits or a combination of both More specifically whichelements contribute most to the overall ray length To clarify thisand inspect how each of the individual elements of the thumb andray IV contribute to IHPs (Fig 1b) we standardized each lengthrelative to overall body size (approximated by the cube root of itsbody mass BM) creating relative length shape ratios of externalhand proportions (EHPs Supplementary Fig 1) Major trends ofEHP variation between the individuals in our anthropoid sampleare summarized and inspected by means of principal componentsanalysis of extant and fossil individuals (Supplementary Table 3)revealing high EHP heterogeneity in extant hominoids (and innon-hominoid anthropoids Fig 2a Supplementary Fig 1) Inother words there is a clear EHP structure that allows thecharacterization of the hominoid taxa Statistical differences inEHP between each great ape genus hylobatids and humans were

ndash20ndash1000

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10

00

ndash10

4030201000ndash10ndash200

10

20

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80

Pollicalmetacarpal

Pollicaldistal phalanx

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Fourthproximal phalanx

Fourthintermediate phalanx

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Rel

ativ

e le

ngth

Po pygmaeus

Hy lar

G beringei

Pa troglodytes

Ho sapiens

ARA-VP-6500

Ar ramidus S

Pr heseloni

Al seniculus

ARA-VP-6500

Ar ramidus L

T geladaPC 3 (669)

PC

2 (

104

8)

PC 1 (7977)

Theropithecus

Po pygmaeusPo abelii

Papio

Pa troglodytesPa paniscus

NasalisMacaca

Hylobatidae

Ho sapiens

G beringeiG gorilla

CebusAlouatta

Qafzeh 9

Kebara 2MH 2

ARA-VP-6500 SARA-VP-6500 L

Pr heseloni

a b

Mandrillus

Figure 2 | Extrinsic hand proportions of humans and other anthropoid primates (a) Principal components analysis of the body mass-adjusted handlengths (b) Summary of the contribution of each hand element in selected anthropoids Species are arranged by maximum length of ray IV (notice that thethumb does not follow the same trend) ARA-VP-6500 L refers to an iteration of Ar ramidus with an estimated body mass of 508 kg whereas ARA-VP-6500 S uses a smaller estimate of 357 kg

NATURE COMMUNICATIONS | DOI 101038ncomms8717 ARTICLE



established (Po0001) by means of multivariate analysis of var-iance (MANOVA with Bonferroni-corrected post hoc pairwisecomparisons see Supplementary Table 4) Differences amongextant great ape genera are more apparent when the eigenanalysisis carried out exclusively on great ape individuals (SupplementaryFig 3) even revealing significant differences between species ofgorillas (Pfrac14 0014) and chimpanzees (Pfrac14 0047) EHPs ofselected species are depicted to help understand extrememorphologies along the major axes of variation in shape space(Fig 2b) A complex pattern is revealed hylobatids orangutansand chimpanzees (in this order) exhibit longer digits thanhumans but gorillas do not Thumb length follows a ratherdifferent trend hylobatids have both the longest digits and thelongest thumbs whereas Theropithecus displays the shortest digitsbut not the shortest thumbs (rather eastern gorillas do) ForAr ramidus we inspect two different relative shape possibilitiesbased on substantially different but plausible BM estimations508 kg (as a quadruped) and 357 kg (as a biped) Fossil homininsdisplay a modern human pattern but Ar ramidus shows onlyslightly longer or shorter (BM-depending) digits than Pr heseloni(that is it is intermediate between humans and chimpanzees) butin both cases it exhibits shorter thumbs (specifically shorterpollical phalanges Supplementary Table 3) than this fossil ape

and other hominins and occupies a different region of EHPshape space (Fig 2 and Supplementary Fig 2) The observeddifferences in EHP between hominoid taxa cannot be merelyattributed to size-dependent effects (that is allometrySupplementary Fig 4 Supplementary Table 5)

The evolution of human and ape hand proportions Previousobservations on modern ape thoraces and limbs suggest thatliving apes show similar but not identical adaptations toaccommodate similar functional demands related to specializedclimbing and suspension (especially Pan and Pongo) reinforcingthe role of parallelism in ape evolution32122 a phenomenonexplained by common evolutionary developmental pathways inclosely related taxa23 To test this homoplastic hypothesis forsimilarities in hand-length proportions between suspensory taxawe enlist the lsquosurfacersquo method24 which allows inferring thehistory of adaptive diversification in hominoids (and otheranthropoids) using a phylogeny (Fig 3) and phenotypic data inthis case the two major axes of EHP variation among extant andfossil species (accounting for 945 of variance see Fig 4 andSupplementary Table 7) This method models adaptiveevolutionary scenarios by fitting a multi-regime Ornstein

Alouatta belzebulAlouatta palliataAlouatta seniculusCebus albifronsCebus apellaNasalis larvatusMandrillus leucophaeusMandrillus sphinxTheropithecus geladaPapio hamadryasMacaca sylvanusMacaca fascicularisMacaca sinicaMacaca mauraMacaca nigraMacaca silenusMacaca nemestrinaMacaca fuscata

Proconsul heseloni

Hylobates pileatusHylobates lar

Hylobates agilis

Hylobates molochHylobates muelleri

Pongo abeliiPongo pygmaeusGorilla gorillaGorilla beringeiPan paniscusPan troglodytes

Ardipithecus ramidusAustralopithecus sediba

Homo neanderthalensisHomo sapiens

Symphalangus syndactylus

Hom

inoidea

40 30 20 10 0Myr

Hylobatidae

Hom

inidaeC

ercopithecidae

Platyrrhini

Catarrhini

Figure 3 | Time-calibrated phylogenetic tree showing the estimated adaptive regimes in our anthropoid sample Adaptive optima are based on the twomajor axes of extrinsic hand proportions (EHP) variation between extant and fossil species (accounting for 945 of the variation) Branches are colour-coded according to different adaptive regimes (revealing that Pan and Pongo -red edges- are convergent) Clades are colour-coded (circles) as followsbrown platyrrhines dark green cercopithecids purple hylobatids light green orangutans red gorillas orange chimpanzees pink fossil hominins lightblue modern humans The nodes corresponding to the last common ancestor (LCA) of great apes-humans and chimpanzees-humans are highlighted




Uhlenbeck (OU) stabilizing selection model25 to the tip data Thisprocedure allows taxonomic units to undergo shifts towardsdifferent phenotypes (lsquoadaptive peaksrsquo) and can be used toidentify cases where multiple lineages have discovered the sameselective regimes (that is convergence) Regimes are hereunderstood as comprising a group of taxonomic units that areinferred to have similar phenotypes Adaptive peaks can beunderstood as the optimal phenotypic values that characterize thedifferent regimes The advantage of the surface method is that itlocates regime shifts without a prior identification of regimes Themethod hereby fits a series of stabilizing selection models anduses a data-driven stepwise algorithm to locate phenotypic shiftson the tree Thus this method allows to lsquonaivelyrsquo detect instancesof phenotypic convergence in human and ape hand proportionsStarting with an OU model in which all species are attracted to asingle adaptive peak in morphospace lsquosurfacersquo uses a stepwisemodel selection procedure based on the finite-samples Akaikeinformation criterion (AICc)2627 to fit increasingly complexmulti-regime models At each step a new regime shift is added tothe branch of the phylogeny that most improves model fit acrossall the variables inspected and shifts are added until no furtherimprovement is achieved To verify true convergence thismethod then evaluates whether the AICc score is further

improved by allowing different species to shift towards sharedadaptive regimes rather than requiring each one to occupy itsown peak For the EHPs lsquosurfacersquo detects five adaptive optima(see edge colours in phylogenetic tree in Fig 3) corresponding to(1) Cebus and Alouatta (2) Papio and Theropithecus (3) MacacaMandrillus Nasalis Gorilla and hominins (4) hylobatids and (5)Pan and Pongo In other words in terms of human and great apeevolution lsquosurfacersquo identifies convergent evolution between theEHPs of Pan and Pongo whereas Gorilla and hominins share amore plesiomorphic condition for catarrhines To verify thisresult we compare the statistical fit of this evolutionary scenariowith that of five other evolutionary hypotheses based on therespective relative AICc weights (Supplementary Fig 5Supplementary Table 8) The alternative models includeBrownian motion evolution a single-regime OU model amulti-regime OU model differentiating the different clades andmost importantly an alternative version of the five-regime OUmodel detected by lsquosurfacersquo in which the condition shared by Panand Pongo is hypothesized to represent the plesiomorphic statefor great apes (OU5 lsquoaltrsquo in Supplementary Fig 5) Our resultssupport the lsquosurfacersquo output as the best fit model using either alarge or a small body size estimate for Ar ramidus (DAICcfrac14 000AICc weightfrac14 100) and even when excluding Ar ramidus and

minus10 minus5 0 5 10 15 20

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5

PC 1 (8621)

PC

2 (

830

)

b

Ar ramidus

Ar ramidus

minus10 minus5 0 5 10 15 20

ndash50

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PC 1 (8634)

PC

2 (

818

)

Al belzebul Al palliata Al seniculus

C albifrons C apella

N larvatus

Man leucophaeus Man sphinx

T gelada

Pap hamadryas

Pr heseloni

S syndactylus

Hy pileatus

Hy lar

Hy agilisHy molochHy muelleri

Po abelii Po pygmaeusG gorilla

G beringei Pa paniscus

Pa troglodytes

Ho sapiens

Honeanderthalensis

Au sediba

Root

a

Great ape-human LCA

Chimpanzee-humanLCA

(+ 95 CI)

(Ar ramidus = 357 kg)

0

10

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60Relative length

Pa troglodytes

Ho sapiens

Chimpanzee-

human LCA


Chimpanzee-

human LCA

0

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50

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Pa troglodytes

Ho sapiens

Relative length

c

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Figure 4 | The evolutionary history of human and ape hand proportions Phylomorphospace projection of the phylogeny presented in Fig 3 onto the twofirst principal components (PCs) of extrinsic hand proportions (EHP) in extant and fossil species Taxa are colour-coded as in the phylogenetic tree internalnodes (that is ancestral-states reconstructed using maximum likelihood) are also indicated highlighting the positions in shape space of the greatape-human and chimpanzee-human LCAs (plus 95 confidence intervals for the latter estimate) (a) EHP of Ardipithecus ramidus estimated using 508 kgOwing to space constrictions macaque species are not labelled (b) Iteration using 357 kg for Ar ramidus Outlines (scaled to similar length) of extant andfossil apes and Ar ramidus are plotted in this phylomorphospace to help visualizing major shape changes occurred during ape and human hand evolutionPanels (c) and (d) depict the EHP of chimpanzees and humans vis-a-vis their reconstructed last common ancestor (LCA) assuming respectively 508 kgand 357 kg for Ar ramidus




Pr heseloni from the analysis (DAICcfrac14 000 AICc weightfrac14 077)To test the sensitivity of our results to a possible sampling biasdue to the higher number of hominoid species in comparisonwith monkey clades in our sample we repeat the analysis oncemore after excluding the most speciose and morphologicallyderived group of hominoids (the hylobatid species) together withthe fossil closest to the hominoid LCA in our sample (that isPr heseloni) Again lsquosurfacersquo identifies a best fit model in whichPan and Pongo are convergent with the difference that theslightly reduced digits of gorillas and hominins are nowinterpreted as being convergent with baboons while theremaining monkey taxa share a common more plesiomorphicregime (Supplementary Fig 6) This evolutionary scenario alsohas the best support (DAICcfrac14 000 AICc weightfrac14 092) whencompared with Brownian motion and four other alternativeevolutionary scenarios (Supplementary Table 8) Importantly interms of human and ape evolution irrespective of the differencein results between the full vs reduced hominoid samplethe similarities between the EHP of hominins and gorillas arereconstructed as representing the plesiomorphic condition for theAfrican ape and human clade (Fig 3) while Pan would be morederived (and convergent with Pongo)

Furthermore to visually track major evolutionary changesdriving differences between apes and humans we summarize theevolutionary history of hominoid hand length diversification (ascompared with platyrrhine and cercopithecid monkey out-groups) by means of a phylomorphospace approach28 Theseare the steps that we followed First we reconstructedhypothetical ancestral morphologies (that is internal nodes inFig 3) using a maximum likelihood approach and plotted themon the shape space defined by the two major EHP axes ofvariation among extant and fossil species (Fig 4) Second wemapped our time-calibrated phylogenetic tree (Fig 3) onto thisshape space by connecting the ancestral sate reconstructions andthe terminal taxa The lengths and orientations of the branches ofthis phylomorphospace allows one to intuitively visualize themagnitude and directionality of inferred shape changes alongeach branch of the tree Owing to the possible impact ofAr ramidus in the reconstruction of the chimpanzee-human LCA(based on its proximity in time) we present this analysis withboth large and small body size estimates (Fig 4ab respectively)as well as by excluding Ar ramidus and Pr heseloni(Supplementary Fig 7) In all cases major evolutionary changesalong PC1 (B86 of variance see Supplementary Table 7) relateto digital (primarily metacarpal and proximal phalanx)lengtheningshortening (positive and negative valuesrespectively) whereas PC2 (B8 of variance) relates to thumbproximal phalanx (positive values) and digital metacarpal(negative values) lengthening and thereby serves to separateour platyrrhine and catarrhine taxa (especially baboons)Although the position of Ar ramidus in shape space differsdepending on estimated BM the overall evolutionary patternremains constant from moderate digital length digitallengthening has been achieved to different degrees andindependently in chimpanzees orangutans and hylobatids (inthis increasing order with Pan and Pongo sharing the sameadaptive optimum see Fig 3) In contrast hominins and gorillas(especially eastern gorillas) have slightly reduced their digitallengths (although both would still represent the sameevolutionary regime see Fig 3) In terms of thumb evolutiononly a modest reduction in extant great apes and slight elongationin later hominins appears to have occurred It is worth noticingthat irrespective of which Ar ramidus BM estimate is used Panfalls clearly outside of the 95 confident interval for the estimatedchimpanzee-human LCA whereas Ar ramidus is very close to it(Fig 4) as previously suggested229 This supports the idea that

chimpanzees exhibit derived hands in this case convergent withPongo (Fig 3)

This previous phylogenetic patterning observed in our EHPmorphospace (that is homoplasy along PC1 and more clade-specific groups along PC2 see Fig 4) was tested with BlombergrsquosK statistic30 Our results indicate that for PC2 variance isconcentrated among clades (K41 1000 permutationsPfrac14 0001) Alouatta (long thumb proximal phalanx and shortdigital metacarpal) and baboons (reverse condition of howlermonkeys) are situated at opposite extremes and othercercopithecids and hominoids exhibit intermediate values ForPC1 however the variance is concentrated within clades (Ko11000 permutations Pfrac14 0001) indicating that the observedvariance in finger length (that is PC1) is larger than expectedbased on the structure of the tree This supports the idea ofadaptive evolution (that is shape change associated with changein function)31 in hominoid finger length uncorrelated withphylogeny30 In other words finger lengthening has beenachieved homoplastically in different ape lineages (probably inrelation to increased suspensory behaviours) as also revealed byour multi-regime OU modelling (Fig 3 Supplementary Figs 5and 6) and phylomorphospace approach (Fig 4)

To inspect how the addition of more taxa with long fingersaffects our evolutionary reconstructions of digital length werevisit the phylomorphospace after excluding the thumbelements Specifically we incorporate the fossil ape Hispano-pithecus laietanus17 (which does not preserve thumb elementsFig 5andashc) and the suspensory platyrrhine Ateles (which exhibitsonly a vestigial thumb32) Hi laietanus represents the earliestevidence of specialized adaptations for below-branch suspensionin the fossil ape record1733 However its phylogenetic position isnot resolved being alternatively considered as a stem great ape astem pongine or even a stem hominine (Fig 5dndashf) In the fourthray morphospace (Fig 6) PC1 (B92 of varianceSupplementary Table 7) is mainly related positively tometacarpal and proximal phalanx lengths whereas PC2 (B6of variance) is positively related to metacarpal length andnegatively to proximal phalanx length When ancestral statereconstructions and phylogenetic mapping are inspected in thisphylomorphospace the overall evolutionary pattern reflectinghomoplasy in modern (and fossil) ape digital elongation is alsoevident irrespective of the BM estimate of Ar ramidus and thephylogenetic position of Hi laietanus (Fig 6) Specifically theseresults also indicate independent digital elongation (to differentdegrees) in hylobatids orangutans chimpanzees spider monkeysand Hi laietanus Although chimpanzees and Hi laietanusexhibit a similar relative digital length (Supplementary Fig 4b) ithas been achieved by different means In contrast to chimpanzeesand baboons that display long metacarpals relative to proximalphalanges (as revealed by PC1 in Fig 6) Hi laietanus approachesa condition similar to that of howler monkeys by exhibiting longphalanges relative to short metacarpals (as revealed by PC2 inFig 6) Overall these results match the previously recognizedmosaic nature of the Hi laietanus hand morphology17 whichsuggests that its suspensory-related adaptations evolvedindependently from that of other apes More broadly eventhough the living hominoid lineages represent the few remnantsof a much more prolific group during the Miocene22 the evidencepresented above indicate that hominoids constitute a highlydiversified group in terms of hand proportions (as identified inFig 2 Supplementary Fig 1 and Figs 4 and 6)

Finally we reconstruct the evolution of IHPs (see Fig 1) ofhumans and modern apes as having evolved in oppositedirections from moderate IHP similar to those exhibited byPr heseloni (Supplementary Fig 8) On the basis of the previousresults on EHP evolution (Fig 4) this implies that the relatively




50

Cebus albifronsCebus apellaAteles paniscusAteles geoffroyiAlouatta belzebulAlouatta palliataAlouatta seniculusNasalis larvatusMandrillus leucophaeusMandrillus sphinxTheropithecus geladaPapio hamadryasMacaca sylvanusMacaca fascicularisMacaca sinicaMacaca mauraMacaca nigraMacaca silenusMacaca nemestrinaMacaca fuscata

Proconsul heseloniSymphalangus syndactylusHylobates pileatusHylobates larHylobates agilisHylobates molochHylobates muelleri

Hispanopithecus laietanusPongo abeliiPongo pygmaeusGorilla gorillaGorilla beringeiPan paniscusPan troglodytes

Ardipithecus ramidusAustralopithecus sedibaHomo neanderthalensisHomo sapiens

40 30 20 10 0





50 40 30 20 10 0


Proconsul heseloniSymphalangus syndactylusHylobates pileatusHylobates larHylobates agilisHylobates molochHylobates muelleriPongo abeliiPongo pygmaeus

Hispanopithecus laietanusGorilla gorillaGorilla beringeiPan paniscusPan troglodytes


50 40 30 20 10 0

d e f

a b c

Myr MyrMyr

Figure 5 | The hand of the late Miocene ape Hispanopithecus laietanus Its reconstructed hand is displayed in dorsal (a) and palmar (b) views andtogether with its associated skeleton (c) This species represents the earliest specialized adaptations for below-branch suspension in the fossil aperecord33 although its hand combining short metacarpals and long phalanges dorsally oriented hamato-metacarpal and metacarpo-phalangeal jointspresents no modern analogues17 The phylogenetic position of Hispanopithecus is still highly debated stem great ape (d) stem pongine (e) or stemhominine (e) Scale bars represent 10 cm Reconstruction of the IPS 18800 (Hispanopithecus) skeleton in panel (c) reproduced with the permission ofSalvador Moya-Sola and Meike Kohler




long thumb of humans and short thumb of modern apes wouldhave been driven primarily by digital elongationshorteningrather than by drastic changes in thumb length The comparisonof eight multi-regime OU models (Supplementary Table 8)identifies a best fit model (DAICcfrac14 000 AICc weightfrac14 100)based on four different optima in which Cebus and Theropithecusare convergent with AustralopithecusHomo for a relatively long(that is easily opposable) thumb Pan is convergent with Pongoand Nasalis for very short thumbs and hylobatids gorillas andAr ramidus share the putative plesiomorphic lsquomoderatersquocondition for crown apes (Supplementary Fig 9)

DiscussionCollectively our results support several evolutionary scenarioswith profound and far-reaching implications regarding ape andhuman origins (see Supplementary Note 2 for an extendedbackground in this matter) (1) extant apes are heterogeneous interms of hand-length proportions (as inspected by means of theirEHP Fig 2 Supplementary Figs S1ndashS3) a finding contrary to aPan-like ancestor lsquobased on parsimonyrsquo In other words ourresults falsify the view that extant apes and particularly Africanapes constitute a homogeneous group with subtle deviationsfrom a similar allometric pattern (for example ref 34 see alsoour Supplementary Fig 4) This previous idea together with thephylogenetic proximity between Pan and Homo has beencommonly used as support for the hypothesis that homininsevolved from a Pan-like ancestor (for example ref 10) Ourresults and the palaeontological evidence indicating

mosaic-manner evolution of the hominoid skeleton161733should caution us against relying on evolutionary scenarios thatassume that extant apes are good lsquooverallrsquo ancestral models22(2) Low levels of inter-limb integration in hominoids relative toother anthropoids (that is higher postcranial heterogeneity)have been used to claim that during hominoid evolutionnatural selection operated for functional dissociation betweenhomologous pairs of limbs allowing for evolutionarylsquoexperimentationrsquo35 For hand length proportions our resultsindicate that Pan and Pongo are convergent (Fig 3Supplementary Fig 9) whereas hylobatids evolved long digitsin parallel to them but to a larger extent (PC1 in Figs 4 and 6)thus representing extreme outliers (related to their small size andspecialized ricochetal brachiation) Thus in terms of evolution ofdigital elongation we hypothesize that in some ape lineagesnatural selection acted on (co)variation in inter-limb lengths andhand proportions in the context of specialized adaptation forbelow-branch suspension This scenario matches previousevidence suggesting the extant ape lineages survived the lateMiocene ape extinction event because they specialized and wereable to share habitats with the radiating and soon to be dominantcercopithecids2336 (3) Similarities in hand proportions betweenhumans and gorillas and our ancestral African ape reconstruction(Figs 2ndash4) indicate that the possession of very long digits was nota requisite for the advent of knuckle walking (4) Thesesimilarities also indicate that specialized tree climbing was notprecluded in australopiths based on hand length (5) Humanshave only slightly modified finger and thumb lengths sincetheir LCA with Pan (Fig 4 Supplementary Fig 8) probably inrelation to refined manipulation as suggested by the convergentsimilarities with Cebus and Theropithecus (Fig 1 SupplementaryFigs 8 and 9) This probably occurred with the advent of habitualbipedalism in hominins and almost certainly preceded regularstone culture4513

Our results provide a detailed picture on the evolution of thehand that is drawn from a multiple-regime model-fittingapproach that infers the evolutionary scenario that indicates theoptimal statistical fit for the observed differences in handproportions between apes and humans in terms of both thetotal amount and direction of shape changes These results arealso most consistent with previous observations on pervasivehomoplasy and complex evolution of the modern ape post-cranium32135 as well as with the available evidence from fossilapes and early hominins12222937

MethodsIntrinsic hand proportions The IHPs were computed as the ratio between thelong bones of the thumb (metacarpal proximal and distal phalanges) and the longbones of the fourth ray but excluding the distal phalanx which is not wellrepresented in the fossil record (that is metacarpal proximal and intermediatephalanges) A total of 270 modern anthropoids including humans all the speciesof great apes hylobatids as well as cercopithecid and platyrrhine monkeys(Supplementary Table 1) were compared with available fossils (Fig 1) and dif-ferences between extant taxa were tested via ANOVA (with Bonferroni posthoccomparisons Supplementary Table 2) As the emphasis of this work is on theevolution of the human hand comparisons were made to our closest living relatives(that is the great apes) at the species level Hylobatids were pooled at the familylevel and extant non-hominoid anthropoids at the genus level Some of the monkeygroups are represented by small samples (for example Theropithecus Mandrillus)due to the difficulty of finding associated distal phalanges (pollical in this case) inthe museum collections (most of them were apparently lost during the skinningand preparation process) However we still included these taxa because theyprovide relevant phylogenetic background to understanding the evolution of handproportions in apes and humans

The fossil sample included the associated hands of Ar ramidus (ARA-VP-6500)and Au sediba (MH2) whose measurements were taken from published sources214the hands of Homo neanderthalensis (Kebara 2) and fossil Homo sapiens (Qafzeh 9)which were measured from the originals and the fossil ape Proconsul heselonimeasurements of which were also taken from the originals (KNM-KPS 1KNM-KPS 3 and KNM-RU 2036) For Ar ramidus pollical proximal phalanx

minus10 minus5 0 5 10 15 20

minus5

0

5

PC 1 (9283)

PC

2 (

688

)

Al belzebul Al seniculus


N larvatus

Man leucophaeusMan sphinx

T gelada

Pap hamadryas

S syndactylusHy pileatus

Hy lar

Hy agilis

Hy moloch

Hy muelleri

Po abeliiPo pygmaeus

G gorillaG beringei

Pa paniscus

Pa troglodytes

Ar ramidus

Honeanderthalensis

Au sediba

minus10 minus5 0 5 10 15 20

minus5

0

5

PC 1 (9275)

PC

2 (

696

)

Hi laietanusAl palliata

At geoffroyiAt paniscusHo sapiens

Pr heseloni


(Ar ramidus = 357 kg)b

a

Ar ramidus

Great ape-human LCA

Chimpanzee-human LCA

Root

Figure 6 | Reconstructed evolutionary histories of human and ape digitalextrinsic proportions The phylomorphospace approach was limited to thethree long bones of ray IV to include the fossil ape Hispanopithecus laietanusand Ateles species The same analysis was iterated with the large (a) andsmall (b) body mass estimates of Ardipithecus ramidus (finding nodifferences in the overall evolutionary pattern) Internal nodes (that isancestral-state reconstructions) and branch lengths are indicated for threedifferent phylogenetic hypotheses Hi laietanus as a stem great ape (black)a stem pongine (orange) and stem African ape (red) Species names areindicated in (a) with the exception of macaques




length in ARA-VP-6500 was estimated in 257 mm from the pollical proximalphalanxfourth metacarpal proportion in the ARA-VP-72 individual and thefourth metacarpal length in ARA-VP-6500 as in Lovejoy et al 2009 (ref 2) ForPr heseloni the estimated length of the KNM-RU 2036 pollical metacarpal wasextracted from the literature1538 IHP in Pr heseloni was computed from the meanproportions obtained after standardizing each manual element by the BM in thethree specimens (see next section)

Shape analyses of extrinsic hand proportions EHPs were computed for anextant sample of 187 anthropoid primates (Supplementary Table 1) and the fossilsdescribed above by standardizing the length (in mm) of each of the six manualelements (inspected in the IHP) by cube root of the BM (kg) associated with eachindividual As tissue density is very similar in all terrestrial organisms (and closelyapproaches unity) mass can be taken as roughly equivalent to volume and thecube root of BM (lsquothe nominal length of measurersquo) is therefore proportional tolinear lsquosizersquo39ndash41

Major trends in EHP variation between the individuals of our sample wereexamined by means of a principal components analysis carried out on thecovariance matrix (Fig 2 Supplementary Figs 2 and 3 Supplementary Table 3)Differences between groups were tested via MANOVA (and Bonferroni post hoccomparisons Supplementary Table 4) of the first three PCs EHPs were furtherexamined for the fourth ray only (if thumb bones are missing) to include the lateMiocene ape Hispanopithecus laietanus (IPS 18800 Figs 5 and 6) for whichmanual lengths were taken from the original fossil17 As this latter analysis wasrestricted to the fourth ray we also included species of Ateles which shows alsquorudimentaryrsquo thumb32

Allometric regressions We relied on ratios to assess intrinsic and extrinsic handproportions in our sample and thus quantify the actual shape of each individual asa scale-free proportion We favour ratios here over residuals because residualsderived from allometric regressions are not a property inherent to the individualsbut rather are sample-dependent42 However to test whether differences betweenthe hand length proportions in our ape sample could be attributed to size-relatedshape changes (that is allometry) we constructed separate bivaritate plots for thenatural log-transformed lengths of the thumb and fourth ray relative BM(Supplementary Fig 5) Least square regressions were fitted to these dataindependently for the extant hominid genera and hylobatids and grade shifts wereinspected through Bonferroni post hoc comparisons between estimated marginalmeans (Supplementary Table 5) after checking for homogeneity of slopes viaanalysis of covariance (ANCOVA)

Body mass estimation Known BMs (kg) were taken from museum records forthe extant samples whenever available Individuals with recorded BM were used toderive genus-specific regressions of BM on femoral head diameter (FHD in mm)These equations were then used to estimate the BM of additional individuals ofunknown BM from their FHD (for example the Pan-specific regression was usedto estimate the BM of Pan specimens only) Generic regressions are provided inSupplementary Table 6

We also derived our own BM estimates for fossils For example we used aregression of BM on FHD of sex-specific means of a diverse group of lsquosmallhumansrsquo (Supplementary Table 6) to estimate the BM of Au sediba this yielded avalue of 325 kg close to the previous (slightly higher) estimate based on thecalcaneus43 but slightly lower than a previous estimate based on FHD44 The caseof Ar ramidus is more complex first a published FHD is not available for thisspecies although estimated FHD can be bracketed from acetabular diameter45 asapproximately 32ndash37 mm second since Ar ramidus is described as a facultativebiped still practicing above-branch pronograde quadrupedalism237 the mostappropriate reference sample (bipeds versus quadrupeds) for estimates of its BM isopen to question (see also Sarmiento and Meldrum for a different interpretation)46Accordingly we estimated the BM in ARA-VP-6500 twice using alternativeregressions based on chimpanzees (the hominoid quadrupedal reference sample)and the aforementioned lsquosmall humansrsquo (the bipedal training sample) whichyielded values of 508 and 357 kg respectively For Hispanopithecus laietanus (IPS18800) BM estimates using a Pongo or a Pan regression generate very similarresults (369 and 376 kg respectively) therefore an average of these two values wasused which is comparable to previous estimates33 For other hominin fossils a BMestimate based on FHD was available in the literature for Qafzeh 9 (ref 47) andanother prediction based on bi-iliac breadth was used for Kebara 2 (ref 48) For theProconsul heseloni individuals BM estimates using different methods andregressions from various preserved anatomical regions were also available49

Phylogenetic trees The time-scaled phylogeny used in this work is based on aconsensus chronometric tree of extant anthropoid taxa downloaded from 10kTreesWebsite (ver 3 http10ktreesfasharvardedu) which provides phylogeniessampled from a Bayesian phylogenetic analysis of eleven mitochondrial and sixautosomal genes available in GenBank and adding branch lengths dated withfossils50 With the exception of Neanderthals (for which molecular data isavailable) other fossil species were introduced post hoc For these fossil species as acriterion of standardization ghost lineages of one million years were added to the

published age of the fossil Au sediba and Ar ramidus were introduced into thehominin lineage as it is most commonly accepted2951 although controversy existsfor Ar ramidus52ndash54 Pr heseloni is most universally interpreted as a stemhominoid15165556 although others consider it as a stem catarrhine52 There is notgeneral consensus for placement of the late Miocene ape from Spain Hi laietanusIts phylogenetic position is debated between stem great ape57 stem pongine33 orstem hominine55 Therefore we created three different trees including this taxonand reiterated the analyses (Figs 5 and 6)

Multi-regime OU modelling Based on its mathematical tractability the mostfrequently used statistical model of evolution is Brownian motion which assumesthat traits change at each unit of time with a mean change of zero and unknownand constant variance58ndash60 Within Brownian motion the evolution of acontinuous trait lsquoXrsquo along a branch over time increment lsquotrsquo is quantified asdX(t)frac14 sdB(t) where lsquosrsquo constitutes the magnitude of undirected stochasticevolution (lsquos2rsquo is generally presented as the Brownian rate parameter) and lsquodB(t)rsquo isGaussian white noise Although novel phylogenetic comparative methods continueusing Brownian evolution as a baseline model they incorporate additionalparameters to model possible deviations from the pure gradual mode of evolutionassumed by Brownian motion OrnsteinndashUhlenbeck (OU) models incorporatestabilizing selection as a constraint and hereby quantify the evolution of acontinuous trait lsquoXrsquo as dX(t)frac14 a[yX(t)]dtthornsdB(t) where lsquosrsquo captures thestochastic evolution of Brownian motion lsquoarsquo determines the rate of adaptiveevolution towards an optimum trait value lsquoyrsquo (see ref 25) This standard OU modelhas been modified into multiple-optima OU models allowing optima to vary acrossthe phylogeny61 In these implementations the parameters are defined a prioriwhich allows testing the relative likelihood of alternative parameterizations(whereby each parameterization characterizes a different evolutionary scenario thatexplains the evolution of a trait) Importantly this approach allows fittingmultivariate data circumventing issues that stem from iteratively fitting univariatedata These model-fitting approaches are available in the R package lsquoouchrsquo (ref 62)and are particularly powerful in testing the relative likelihood of alternativeevolutionary scenarios explaining multivariate data Although this OU modelfitting approach comprises a powerful way of comparing the likelihood ofalternative evolutionary scenarios it leaves open the possibility that the lsquobest-fitrsquoevolutionary scenario is not included in the research design In this context Ingramamp Mahler (ref 24) expanded the OU model fitting approach by developing a way toestimate the number of shifts and their locations on the phylogeny rather than apriori assuming them This method (lsquosurfacersquo) was developed specifically to identifyinstances of convergent evolution and can be used to extract the evolutionaryscenario that indicates the best statistical fit (that is the lowest Akaike informationcriterion based on the finite samples AICc)2627 between the phylogeny and theobserved measurements We subsequently translated the best fit model fromlsquosurfacersquo to lsquoouchrsquo to compare it with alternative hypotheses in a fully multivariateframework

Phylomorphospace The phylomorphospace approach allows one to visualize thehistory of morphological diversification of a clade and infer the magnitude anddirection of shape change along any branch of the phylogeny28 Thus wereconstructed the evolutionary history of extrinsic hand proportions in apes andhumans (and other anthropoid primates) by projecting our phylogenetic trees(Fig 3 Fig 5def) into our morphospaces (frac14 shape space Figs 4 and 6) based oneigenanalyses of the covariance matrices of the species means (SupplementaryTable 7) This was accomplished by reconstructing the position of the internalnodes (that is ancestral states) using a maximum likelihood (ML) method forcontinuous characters6364 For an evolutionary model based on normallydistributed Brownian motion58ndash60 the ML approach yields identical ancestral stateestimates to the squared-change parsimony method accounting for branch lengthwhich minimizes the total amount shape change along all the branches of thetree6566 In our case our results including (Fig 4) and not including(Supplementary Fig 7) key fossils or using different phylogenetic positions of thesame fossils (Fig 6) were essentially unchanged This suggests that although fossilsare useful to more accurately bound ancestral state reconstructions67 in our casethe overall evolutionary patterns recovered are robust These visualizations werecomputed using the R package lsquophytoolsrsquo (ref 68) 95 confidence intervals(95 CIs) for the last common ancestor (LCA) of chimpanzees and humans werecomputed using the lsquofastAncrsquo function implemented in lsquophytoolsrsquo and are based onequation [6] of Rohlf (ref 69) that computes the variance on the ancestral statesestimates Once these variances are known 95 CIs on the estimates can becomputed as the estimates thorn 196$ the square root of the variances

Phylogenetic signal Phylogenetic signal is generally defined as the degree towhich related species resemble each other6070 We relied on Blombergrsquos Kstatistic30 to assess the amount of phylogenetic signal relative to the amountexpected for a character undergoing Brownian motion This statistic is based on acomparison of the mean squared error of the tip data (measured from thephylogenetic mean) with the mean squared error of the data calculated using thevariance-covariance matrix of the tree This ratio reflects whether the treeaccurately describes the variance-covariance pattern in the data and is




subsequently compared with the expected ratio given the size and the shape of thetree (resulting in the K statistic) When Ko1 close relatives resemble each otherless than expected under Brownian motion thus indicating that variance isconcentrated within clades rather than among clades Ko1 is suggestive of a modeof evolution that departs from pure Brownian motion This departure fromBrownian motion could be caused among others by adaptive evolutionuncorrelated with the phylogeny (that is homoplasy) KB1 indicates that thevariance in the tips accurately reflects phylogenetic relatedness (a mode ofevolution aligning with Brownian motion) When K41 close relatives resembleeach other more than expected under Brownian motion (possibly reflectingstabilizing selection) K is also a measure of the partitioning of variance Thus(with Brownian motion as reference) whether K41 the variance tends to bebetween clades whereas if Ko1 the variance tends to be within clades (LiamRevell personal communication) The statistical significance of K was evaluatedwith the permutation test (1000 iterations) described by Blomberg et al (ref 30)

References1 Napier J Hands 180 (Princeton Univ Press 1993)2 Lovejoy C O Simpson S W White T D Asfaw B amp Suwa G Careful

climbing in the Miocene The forelimbs of Ardipithecus ramidus and humansare primitive Science 326 70ndash708 (2009)

3 Tuttle R in Phylogeny of the Primates (eds Luckett W Patrick amp SzalayFrederick S) 447ndash480 (Springer 1975)

4 Almecija S amp Alba D M On manual proportions and pad-to-pad precisiongrasping in Australopithecus afarensis J Hum Evol 73 88ndash92 (2014)

5 Alba D M Moya-Sola S amp Kohler M Morphological affinities of theAustralopithecus afarensis hand on the basis of manual proportions and relativethumb length J Hum Evol 44 225ndash254 (2003)

6 Schultz A H Characters common to higher primates and characters specificfor man Q Rev Biol 11 259ndash283 (1936)

7 Straus W L Jr The riddle of manrsquos ancestry Q Rev Biol 24 200ndash223 (1949)8 Le Gros Clark W E The Fossil Evidence for Human Evolution 200 (University

of Chicago Press 1964)9 Ruvolo M Disotell T R Allard M W Brown W M amp Honeycutt R L

Resolution of the African hominoid trichotomy by use of a mitochondrial genesequence Proc Natl Acad Sci USA 88 1570ndash1574 (1991)

10 Wrangham R amp Pilbeam D in All Apes Great and Small (eds Galdikas BiruteM F et al) 5ndash17 (Kluwer AcademicPlenum Publishers 2001)

11 Richmond B G Begun D R amp Strait D S Origin of human bipedalism theknuckle-walking hypothesis revisited Yearb Phys Anthropol 44 70ndash105(2001)

12 Rolian C Lieberman D E amp Hallgrımsson B The coevolution of humanhands and feet Evolution 64 1558ndash1568 (2010)

13 Almecija S Moya-Sola S amp Alba D M Early origin for human-like precisiongrasping A comparative study of pollical distal phalanges in fossil homininsPLoS ONE 5 e11727 (2010)

14 Kivell T L Kibii J M Churchill S E Schmid P amp Berger L RAustralopithecus sediba hand demonstrates mosaic evolution of locomotor andmanipulative abilities Science 333 1411ndash1417 (2011)

15 Napier J R amp Davis P R The fore-limb skeleton and associated remains ofProconsul africanus Foss Mamm Afr 16 1ndash69 (1959)

16 Moya-Sola S Kohler M Alba D M Casanovas-Vilar I amp Galindo JPierolapithecus catalaunicus a new Middle Miocene great ape from SpainScience 306 1339ndash1344 (2004)

17 Almecija S Alba D M Moya-Sola S amp Kohler M Orang-like manualadaptations in the fossil hominoid Hispanopithecus laietanus first steps towardsgreat ape suspensory behaviours Proc Biol Sci 274 2375ndash2384 (2007)

18 Almecija S Alba D M amp Moya-Sola S Pierolapithecus and the functionalmorphology of Miocene ape hand phalanges paleobiological and evolutionaryimplications J Hum Evol 57 284ndash297 (2009)

19 Schultz A H The skeleton of the trunk and limbs of higher primates HumBiol 2 303ndash438 (1930)

20 Christel M in Hands of Primates (eds Preuschoft Holger amp Chivers David J)91ndash108 (Springer 1993)

21 Larson S G Parallel evolution in the hominoid trunk and forelimb EvolAnthropol 6 87ndash99 (1998)

22 Almecija S et al The femur of Orrorin tugenensis exhibits morphometricaffinities with both Miocene apes and later hominins Nat Commun 4 2888(2013)

23 Reno P L Genetic and developmental basis for parallel evolution and itssignificance for hominoid evolution Evol Anthropol 23 188ndash200 (2014)

24 Ingram T amp Mahler D L SURFACE detecting convergent evolution fromcomparative data by fitting Ornstein-Uhlenbeck models with stepwise AkaikeInformation Criterion Methods Ecol Evol 4 416ndash425 (2013)

25 Hansen T F Stabilizing selection and the comparative analysis of adaptationEvolution 51 1341ndash1351 (1997)

26 Akaike H A new look at the statistical model identification IEEE TransactAutomatic Control 19 716ndash723 (1974)

27 Hurvich C M amp Tsai C-L Regression and time series model selection insmall samples Biometrika 76 297ndash307 (1989)

28 Sidlauskas B Continuous and arrested morphological diversification in sisterclades of characiform fishes A phylomorphospace approach Evolution 623135ndash3156 (2008)

29 White T D et al Ardipithecus ramidus and the paleobiology of earlyhominids Science 326 64ndash86 (2009)

30 Blomberg S P Garland T Jr amp Ives A R Testing for phylogeneticsignal in comparative data behavioral traits are more labile Evolution 57717ndash745 (2003)

31 Gould S J amp Vrba E S Exaptation-a missing term in the science of formPaleobiology 8 4ndash15 (1982)

32 Straus W L Jr Rudimentary digits in primates Q Rev Biol 17 228ndash243(1942)

33 Moya-Sola S amp Kohler M A Dryopithecus skeleton and the origins of great-ape locomotion Nature 379 156ndash159 (1996)

34 Shea B T Allometry and heterochrony in the African apes Am J PhysAnthropol 62 275ndash289 (1983)

35 Young N M Wagner G P amp Hallgrımsson B Development and theevolvability of human limbs Proc Natl Acad Sci USA 107 3400ndash3405 (2010)

36 Jablonski N G Whitfort M J Roberts-Smith N amp Qinqi X The influence oflife history and diet on the distribution of catarrhine primates during thePleistocene in eastern Asia J Hum Evol 39 131ndash157 (2000)

37 Lovejoy C O Latimer B Suwa G Asfaw B amp White T D Combiningprehension and propulsion The foot of Ardipithecus ramidus Science 32672ndash728 (2009)

38 Walker A C amp Pickford M in New Interpretations of Ape and HumanAncestry (eds Ciochon R L amp Corruccini R S) 325ndash351 (Plenum Press1983)

39 Sneath P H amp Sokal R R Numerical Taxonomy The Principles and Practiceof Numerical Classification (1973)

40 Jungers W L in Size and Scaling in Primate Biology (ed Jungers W L)345ndash381 (Plenum Press 1985)

41 Vogel S Lifersquos Devices the Physical World of Animals and Plants (PrincetonUniv Press 1988)

42 Jungers W L Falsetti A B amp Wall C E Shape relative size and size-adjustments in morphometrics Yearb Phys Anthropol 38 137ndash161 (1995)

43 Zipfel B et al The foot and ankle of Australopithecus sediba Science 3331417ndash1420 (2011)

44 de Ruiter D J Churchill S E amp Berger L R in The Paleobiology ofAustralopithecus 147ndash160 (Springer 2013)

45 Plavcan J M Hammond A S amp Ward C V Brief CommunicationCalculating hominin and nonhuman anthropoid femoral head diameter fromacetabular size Am J Phys Anthropol 155 469ndash475 (2014)

46 Sarmiento E E amp Meldrum D J Behavioral and phylogenetic implications ofa narrow allometric study of Ardipithecus ramidus HOMO 62 75ndash108 (2011)

47 Trinkaus E amp Ruff C Femoral and tibial diaphyseal crosssectional geometryin Pleistocene Homo PaleoAnthropology 13 62 (2012)

48 Ruff C Niskanen M Junno J-A amp Jamison P Body mass prediction fromstature and bi-iliac breadth in two high latitude populations with application toearlier higher latitude humans J Hum Evol 48 381ndash392 (2005)

49 Rafferty K L Walker A Ruff C B Rose M D amp Andrews P J Postcranialestimates of body weight in Proconsul with a note on a distal tibia of P majorfrom Napak Uganda Am J Phys Anthropol 97 391ndash402 (1995)

50 Arnold C Matthews L J amp Nunn C L The 10kTrees website A new onlineresource for primate phylogeny Evol Anthropol 19 114ndash118 (2010)

51 Berger L R et al Australopithecus sediba A new species of Homo-likeaustralopith from South Africa Science 328 195ndash204 (2010)

52 Harrison T Apes among the tangled branches of human origins Science 327532ndash534 (2010)

53 Wood B amp Harrison T The evolutionary context of the first hominins Nature470 347ndash352 (2011)

54 Sarmiento E E Comment on the paleobiology and classification ofArdipithecus ramidus Science 328 1105-b (2010)

55 Begun D R Nargolwalla M C amp Kordos L European Miocene hominidsand the origin of the African ape and human clade Evol Anthropol 21 10ndash23(2012)

56 Rossie J B amp MacLatchy L A new pliopithecoid genus from the early Mioceneof Uganda J Hum Evol 5 568ndash586 (2006)

57 Perez de los Rıos M Moya-Sola S amp Alba D M The nasal and paranasalarchitecture of the Middle Miocene ape Pierolapithecus catalaunicus (primatesHominidae) Phylogenetic implications J Hum Evol 63 497ndash506 (2012)

58 Cavalli-Sforza L L amp Edwards A W Phylogenetic analysis Models andestimation procedures Am J Hum Genet 19 233 (1967)

59 Felsenstein J Maximum-likelihood estimation of evolutionary trees fromcontinuous characters Am J Hum Genet 25 471 (1973)

60 Felsenstein J Phylogenies and the comparative method Am Nat 125 1ndash15(1985)




61 Butler M A amp King A A Phylogenetic comparative analysis a modelingapproach for adaptive evolution Am Nat 164 683ndash695 (2004)

62 King A A amp Butler M A ouch Ornstein-Uhlenbeck models for phylogeneticcomparative hypotheses (R package) httpouchr-forger-projectorg (2009)

63 Felsenstein J Phylogenies and quantitative characters Annu Rev Ecol Syst19 445ndash471 (1988)

64 Schluter D Price T Mooers A Oslash amp Ludwig D Likelihood of ancestor statesin adaptive radiation Evolution 51 1699ndash1711 (1997)

65 Rohlf F J in Morphology Shape and Phylogeny (eds MacLeod N amp Forey P L)175ndash193 (Taylor and Francis 2002)

66 Maddison W P Squared-change parsimony reconstructions of ancestral statesfor continuous-valued characters on a phylogenetic tree Syst Zool 40 304ndash314(1991)

67 Slater G J Harmon L J amp Alfaro M E Integrating fossils with molecularphylogenies improves inference of trait evolution Evolution 66 3931ndash3944(2012)

68 Revell L J Phytools an R package for phylogenetic comparative biology (andother things) Methods Ecol Evol 3 217ndash223 (2012)

69 Rohlf F J Comparative methods for the analysis of continuous variablesgeometric interpretations Evolution 55 2143ndash2160 (2001)

70 Harvey P H amp Pagel M D The Comparative Method in Evolutionary BiologyVol 239 (Oxford univ press 1991)

AcknowledgementsWe are indebted to the following researchers and curators for granting access tocollections under their care Emma Mbua National Museum of KenyaSalvador Moya-Sola Institut Catala de Paleontologia Miquel Crusafont Yoel RakTel Aviv University Emmanuel Gilissen Royal Museum of Central Africa EileenWestwig American Museum of Natural History Lyman Jellema Cleveland Museum ofNatural History Darrin Lunde National Museum of Natural History Judy ChupaskoMuseum of Comparative Zoology and Randy Susman Stony Brook University We are

also grateful to Liam Revell for technical advice to David Alba Biren Patel and SteveFrost for helping compiling the data and to Matt Tocheri Caley Orr and Biren Patel forfeedback in previous versions of this work This research was supported by the NationalScience Foundation (NSF-BCS 1316947 NSF-BCS-1317047 NSF-BCS 1317029) theSpanish Ministerio de Economıa y Competitividad (CGL2014-54373-P) the IreneLevi Sala CARE Archaeological Foundation (SA) and the AAPA ProfessionalDevelopment Grant (SA)

Author contributionsSA designed the study SA and WLJ collected the data and performed the morpho-metric analyses SA and JBS performed the evolutionary analyses SA JBS andWLJ discussed the results and wrote the paper

Additional informationSupplementary Information accompanies this paper at httpwwwnaturecomnaturecommunications

Competing financial interests The authors declare no competing financial interests

Reprints and permission information is available online at httpnpgnaturecomreprintsandpermissions

How to cite this article Almecija S et al The evolution of human and ape handproportions Nat Commun 67717 doi 101038ncomms8717 (2015)

This work is licensed under a Creative Commons Attribution 40International License The images or other third party material in this

article are included in the articlersquos Creative Commons license unless indicated otherwisein the credit line if the material is not included under the Creative Commons licenseusers will need to obtain permission from the license holder to reproduce the materialTo view a copy of this license visit httpcreativecommonsorglicensesby40




ͳ

Supplementary Figure 1 | Extrinsic hand proportions of humans apes and other anthropoid primates Species means are displayed for all extant hominid species selected hylobatids and one species representative of each non-hominoid anthropoid genus Each element length (in mm) has been adjusted by the known or estimated cube root of body mass (in kg) of the individual This plot demonstrates the huge disparity in hand proportions among extant hominoids In comparison to humans chimpanzees have longer digits and slightly shorter thumbs contrarily gorillas exhibit similar digital length but shorter thumbs orangutans display longer fingers (longer than chimpanzees) and slightly shorter thumbs finally hylobatids exhibit much longer digits and thumbs Other relevant observations in non-hominoids Theropithecus approaches the human intrinsic hand proportions (Fig 1b) by a different mechanism (longer pollical and digital metacarpals but much shorter phalanges) Nasalis exhibits chimpanzee-like digital length with a shorter thumb but African colobines (not included) would exhibit even shorter ones (they display vestigial thumb elements) Fossil species are indicated (dagger)

ʹ

Supplementary Figure 2 | Principal components analysis of extrinsic hand proportions in humans apes and other anthropoid primates The results displayed in the three-dimensional plot of Figure 2a are depicted here in two dimensions a Principal component 1 (PC1) and PC2 b PC1 and PC3 For Ardipithecus ramidus the two body mass-dependent iterations were introduced in the analysis as different operational taxonomic units ARA-VP-6500 L (508 kg) and ARA-VP-6500 S (357 kg) PC1 (7977 of variance Supplementary Information section 33) is related especially to digital length (all elements of ray fourth in this case) and its opposite extremes are represented by the hominins gorillas and baboons (short digits) on one hand and hylobatids (very long digits) on the other PC2 (1048 of variance) is positively related to pollical phalangeal length hominins (with the exception of both iterations of Ar ramidus) hylobatids Proconsul heseloni and especially platyrrhines exhibit longer pollical phalnages than extant great apes and especially baboons (exhibiting the shortest thumbs) PC3 (669 of variance) is negatively related to pollical metacarpal length hominins (again with the exception of Ar ramidus) but especially baboons and hylobatids exhibit longer pollical metacarpals than great apes Each great ape genus hylobatids and humans exhibit statistical differences in EHP (Plt0001 MANOVA Supplementary Table 4)

͵

Supplementary Figure 3 | Principal components analysis of extrinsic hand proportions in extant great ape species The combination of the two first principal components (accounting for gt96 of total shape variance Supplementary Table 3) distinguishes the three extant genera (with just a slight overlap between Pan and Pongo) PC1 (9237 of variance) is related to overall length of digit fourth and thumb (excluding the pollical distal phalanx) and completely separates gorillas (short digits and thumb) from chimpanzees and especially orangutans PC2 (379 of variance) is strongly related to pollical distal phalanx length and reveals a cline (from shorter to longer) with statistically significant differences between eastern and western gorillas (ANOVA P=0014) as well as between common and pygmy chimpanzees (P=0047)

Ͷ

Supplementary Figure 4 | Allometric relationships of thumb (a) and fourth ray (b) lengths relative to body mass (BM) in humans and other anthropoid primates In both cases regression lines are fitted to hylobatids (purple) orangutans (light green) gorillas (red) chimpanzees (orange) and modern humans (light blue) and extended over the remaining comparative sample Analyses of covariance (ANCOVA) show that there are not significant differences in the slopes of the thumb (F=1954 P=0107) and fourth ray (F=1131 P=0343) regressions However in both cases modern humans show regression slopes that are not statistically different from zero (Supplementary Table 5) indicating that in humans thumb and digital lengths are not dependent on body size Comparisons between pollical marginal means (evaluated at lnBM=3796) reveal that modern humans and hylobatids (not statistically different) exhibit longer thumbs than great apes (Plt0001) Gorillas display even shorter thumbs (P=0001) than chimpanzees and orangutans (the latter two showing no differences) Comparisons between fourth ray marginal means (evaluated at lnBM=3828) reveal differences between each ape group and humans (P0008) with the exception of chimpanzees and hylobatids (P=0332) When accounting for allometric relationships orangutans exhibit longer fourth ray than hylobatidschimpanzees which in turn are longer than gorillas and humans respectively

ͷ

Supplementary Figure 5 | Alternative multivariate multi-regime Ornstein-Uhlenbeck (OU) hypotheses tested for the evolution of extrinsic hand proportions (EHP) Starting with Brownian motion as a baseline we compared the relative fit (using AICc) of increasingly complex OU models with ldquoouchrdquo one single regime (OU1) two regimes (OU2 hominoids vs non-hominoids) four regimes (OU4 platyrrines cercopithecids non-human hominoids plus Ardipithecus Australopithecus-Homo) the five regimes revealed by ldquosurfacerdquo (OU5 lsquosurfacersquo platyrrhines Papio-Theropithecus hylobatids Pan-Pongo rest of catarrhines) We further designed an alternative version of the previous model (OU5 lsquoaltrsquo) in which Pan and Pongo were considered to reflect the plesiomorphic great ape condition The OU5 lsquosurfacersquo model represented the best fit model irrespective of the body mass estimate used for Ardipithecus and the inclusion or not of Ardipithecus and Proconsul (see results in Supplementary Table 8)

Supplementary Figure 6 | Sensitivity test of species sample size in alternative multivariate multi-regime Ornstein-Uhlenbeck (OU) models of extrinsic hand proportions evolution We compared the fit of different OU models after dropping all hylobatid species and Proconsul Alternative hypotheses included the OU1 OU2 and OU4 models described in Supplementary Figure 5 plus the three regime output revealed by ldquosurfacerdquo (OU3 lsquosurfacersquo) and an alternative version of OU3 lsquosurfacersquo (OU4 lsquoaltrsquo) based on the best fit model obtained for the full sample (Supplementary Fig 5) In this case the best fit model is represented by the OU3 lsquosurfacersquo output in which upon an anthropoid regime baseline hominins and gorillas share an optimum (convergent with baboons) whereas Pan and Pongo are again convergent (see results in Supplementary Table 8)

7

minus10 minus5 0 5 10 15 20

minus50

5

PC 1 (8651)

PC 2

(82

6)



N larvatus


T geladaPap hamadryas

S syndactylus

Hy pileatus

Hy lar

Hy agilis Hy molochHy muelleri

Po abelii Po pygmaeus G gorilla


Pa troglodytes

Ho sapiens

Honeanderthalensis

Au sediba

great ape-human LCA

chimpanzee-humanLCA

(+ 95 CI)

Root

Supplementary Figure 7 | Reconstructed evolutionary history of human and ape hand proportions by excluding contentious fossils Same approach as in Figure 4 but excluding Proconsul heseloni and Ardipithecus ramidus Taxa are color-coded as in the phylogenetic tree (Fig 3) internal nodes (ie ancestral-state reconstruction) are also indicated highlighting the positions in shape-space of the great ape-human and chimpanzee-human LCA (plus 95 confident intervals for the latter estimate) The overall evolutionary pattern is comparable to that found in previous iterations including more fossils Again species of macaques were not labelled due to space restrictions

ͺ

Supplementary Figure 8 | Evolution of intrinsic hand proportions (IHP) in humans and other anthropoid primates The observed (Fig 1) and reconstructed-state values are mapped along the branches and nodes of the anthropoid phylogeny The ancestral state values for the great ape-human and chimpanzee-human last common ancestors (LCA) are highlighted with arrows The IHP (relative long thumb) of humans geladas and capuchin monkeys as well as the IHP (different degrees of relative short thumb) of modern apes and Nasalis are reconstructed as having evolved (independently) from moderate proportions similar to Proconsul Inset drawing represents a modern human performing a ldquopad-to-padrdquo precision grasping1 The length of the color legend at the bottom provides scale for the branches of the tree

ͻ

Supplementary Figure 8 | Continued This method to visualize trait evolution in a tree is explained in detail elsewhere2 Basically ancestral characters are first estimated at the internal nodes again using ML34 and Brownian motion5-7 Next all edges along the tree are fractionated and state estimates are computed at the midpoint of each fraction via interpolation using equation [3] of Felsenstein7 This creates the visual appearance of continuous color change along the edges of the tree

ͳͲ

Supplementary Figure 9 | Alternative multi-regime Ornstein-Uhlenbeck (OU) hypotheses tested for the evolution of intrinsic hand proportions (IHP) In total we compared the relative fit of eight different OU multi-regime models Starting with Brownian motion we followed with the increasingly complex models OU1 OU2 OU4 as well as the best fit model for extrinsic hand proportions described in Supplementary Figure 5 Furthermore we incorporated three extra models (this figure) based on the IHP results revealed by Figure 1 and Supplementary Figure 8 (as expected ldquosurfacerdquo did not perform well with univariate data8) The four adaptive regimes OU4 lsquoIHPrsquo represented the best fit model Australopithecus-Homo share an adaptive regime with Theropithecus and Cebus (ie they are convergent for a relative long thumb) Pan and Pongo are convergent for a relative short thumb (as in the case of extrinsic hand proportions Supplementary Fig 5) as well as Nasalis hylobatids gorillas and Ardipithecus share the inferred plesiomorphic condition for crown apes whereas the rest of the cercopithecid and platyrrhine monkeys share a more generalized regime Alternative models in which Pan Pongo and Nasalis share the same regime as other hominoids (OU3 lsquoIHP alt1rsquo) or where Theropithecus and Cebusare not convergent with Australopithecus-Homo (OU4 lsquoIHP alt2rsquo) exhibited an inferior fit (see results in Supplementary Table 8)

ͳͳ

Supplementary Table 1 | Samples of extant primates used in each analysis Non-hominoid sample continues in the following page

taxon N species IHP EXPHomo 40 Ho sapiens a 40 15 Pan 46 Pa troglodytes b 34 30

Pa paniscus c 12 10 Gorilla 34 G beringei d 21 14

G gorilla e 13 7 Pongo 27 Po pygmaeus f 19 15

Po abelii g 8 8 Hylobatidae 14 Hy agilis h 2 1

Hy muelleri h 2 1 Hy moloch h 3 1 Hy lar i 4 4 Hy pileatus j 1 1 S syndactylus k 2 2

ͳʹ

Supplementary Table 1 | Continued

taxon N species IHP EXP Macaca 18 Ma fuscata h 2 2

Ma nemestrina h 4 4 Ma silenus h 2 2 Ma nigra h 2 2 Ma maura h 1 1 Ma sinica h 1 1 Ma fascicularis h 3 3 Ma sylvanus h 3 3

Papio 50 Pap hamadryas l 50 22 Theropithecus 5 T gelada m 5 4 Mandrillus 3 Man sphinx n 2 2

Man leucophaeus h 1 1 Nasalis 14 Nasalis larvatus i 14 11 Cebus 11 C apella j 3 3

C albifrons o 6 5 C sp o 2 0

Alouatta 8 Al seniculus j 5 5 Al palliata h 2 2 Al belzebul h 1 1

Ateles 4 At geoffroyi h 0 2 At paniscus h 0 2

Total 274 270 187 Superscripts indicate the collection provenience for each taxon (a) CMNH (b) AMNH Naturalis RMCA SBU (c) RMCA SBU (d) AMNH NRM RMCA USNM (e) AMNH PC (f) AMNH MCZ Naturalis USNM (g) CMNH Naturalis USNM (h) Naturalis (i) MCZ Naturalis (j) AMNH (k) AMNH Naturalis (l) AMNH KNM Naturalis RMCA SBU USNM (m) AMNH NME SBU (n) Naturalis RMCA (o) AMNH SBU Abbreviations N (total sample size for genus) IHP (sample size for intrinsic hand proportions) EXP (sample size for extrinsic hand proportions) AMNH (American Museum of Natural History) CMNH (Cleveland Museum of Natural History) KNM (Kenya National Museums) MCZ (Museum of Comparative Zoology) Naturalis (Naturalis Biodiversity Center) NME (National Museum of Ethiopia) NRM (Swedish Museum of Natural History) PC (Powell-Cotton Museum) RMCA (Royal Museum of Central Africa) SBU (Stony Brook University) USNM (National Museum of Natural History)

ͳ͵

Supplementary Table 2 | Intrinsic hand proportions Bonferroni-corrected pairwise post hoc comparisons

Pa paniscus Pa troglodytes G gorilla G beringei Po abelii Po pygmaeus Ho sapiens Hylobatidae Papio Theropithecus Mandrillus Macaca Nasalis Cebus

Pa troglodytes 1000

G gorilla 0031 0000

G beringei 0000 0000 1000

Po abelii 0000 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0208 0000 1000 1000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0000 0000 0000 0000 0012 0000 0000

Mandrillus 0000 0000 0000 0001 0000 0000 0000 0000 1000 0000

Macaca 0000 0000 0002 0269 0000 0000 0000 0000 0597 0000 0520

Nasalis 0516 1000 0000 0000 0123 0000 0000 0000 0000 0000 0000 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 1000 0000 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0008 0000 1000 0000 0000 0000

Significant differences (Plt005) are marked in bold

ͳͶ

Supplementary Table 3 | Results of the principal component analyses (PCA) Results are shown for the individuals-based extrinsic hand proportions in our full (Fig 2A Supplementary Fig 2) and great apes only samples (Supplementary Fig 3)

PCA full sample PCA great apes PC1 PC2 PC3 PC1 PC2

var 7977 1049 669 9238 379 var cumulative 7977 9026 9695 9238 9617

MC1L 066 018 -070 091 013 PP1L 051 080 -023 076 041 DP1L 023 070 -015 038 072 MC4L 095 -030 -007 099 012 PP4L 096 018 019 097 -021 IP4L 094 022 022 097 -006

Data is provided only for the axes accounting for most of the variance which are displayed in the plots Loadings with absolute values 05 are marked in bold Abbreviations MC metacarpal PP proximal phalanx DP distal phalanx IP intermediate phalanx L length Each length was divided by the cube root of body mass

ͳͷ

Supplementary Table 4 | Extrinsic hand proportions Bonferroni-corrected post hoc pairwise comparisons (Hotellingrsquos p-values)


Pa troglodytes 1000

G gorilla 0005 0000

G beringei 0000 0000 1000

Po abelii 0005 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0000 0000 0000 0000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0004 0000 0000 0000 0000 0000 0000

Mandrillus 0043 0000 0508 0002 0007 0000 0001 0005 0004 1000

Macaca 0000 0000 0018 0000 0000 0000 0000 0000 0000 0000 0234

Nasalis 0001 0000 0001 0000 0001 0000 0000 0000 0000 0000 0002 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0002 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0001 0000 0000 0000

Comparisons based in the three first principal components which account for ~97 of the total variance Significant differences (Plt005) are marked in bold

ͳ

Supplementary Table 5 | Allometric regressions of thumb and fourth ray lengths (mm) relative to body mass (kg) in modern hominoids N R SEE p slope 95 CI intercept 95 CI

Thumb Pan 41 0562 0043 0000 0183 0096 0271 3753 3428 4078 Gorilla 21 0897 0033 0000 029 0221 0359 3162 2827 3497 Pongo 23 0809 0037 0000 0232 0156 0308 3573 3278 3869 Homo 15 0328 0102 0233 0128 -0093 0349 4113 3271 4955

Hylobatidae 10 0657 0052 0039 0128 0008 0248 3956 3735 4178 Ray IV Pan 66 0704 0031 0000 0247 0185 031 4235 4002 4468

Gorilla 44 0801 0025 0000 0213 0163 0262 4164 3926 4403 Pongo 36 0776 0026 0000 0185 0132 0237 464 4436 4844 Homo 16 0381 0093 0145 0143 -0056 0342 4308 3551 5065

Hylobatidae 21 0813 0027 0000 0166 0109 0223 4538 4425 4651 Significant slopes (ie statistically different from zero) are marked in bold Humans are the only hominoids without predictable covariation between hand lengths and body size

ͳ

Supplementary Table 6 | Least-squares regressions of body mass (BM kg) on femoral head diameter (FHD mm) Regressions at the genus level in small modern humans and wild-shot primates N R SEE BM prediction Pan (troglodytes and paniscus) 28 083 610 3287 x FHD ndash 6262 Gorilla (gorilla and beringei) 14 091 1990 7843 x FHD ndash 23603 Pongo (abelli and pygmaeus) 19 094 790 5265 x FHD ndash 12363 Homo (ldquosmall humansrdquo) 088 217 1747 x FHD ndash 24602Hylobatidae (Hy lar and S syndactylus) 18 093 110 1176 x FHD ndash 1296 Papio hamadryas 35 091 260 2466 x FHD ndash 3517 Macaca (fascicularis and nemestrina) 21 089 080 0856 x FHD ndash 618 Nasalis larvatus 10 095 210 1907 x FHD ndash 236 Cebus (apella and albifrons) 30 067 056 1078 x FHD ndash 8036 Alouatta (seniculus and caraya) 15 089 074 1156 x FHD ndash 9816 The ldquosmall humanrdquo regression is based in ten sex-specific population means including Eastern and Western African pygmies Khoe-San Aeta and Andaman Islanders Supplementary Table 7 | Results of the principal component analyses (PCA) using the covariance matrix between species means Results are provided for the full set of extrinsic hand proportions (Fig 4a b) and for the fourth ray only (Fig 6ab) Each analysis was iterated with a large (ArdiL 508 kg) and small (ArdiS 357 kg) body mass estimate for Ar ramidus

ArdiL ArdiS Hispano-ArdiL Hispano-ArdiS PC1 PC2 PC1 PC2 PC1 PC2 PC1 PC2

var 8634 818 8621 830 9283 688 9275 696 var cumulative 8634 9452 8621 9451 9283 9971 9275 9971

MC1L 032 -015 031 -016 PP1L 018 053 018 053DP1L 006 034 006 034 MC4L 066 -059 066 -059 070 071 070 071 PP4L 053 039 053 039 057 -057 057 -057 MP4L 039 030 039 030 042 -042 042 -042


ͳͺ

Supplementary Table 8 | Results of alternative multivariate multi-regime Ornstein-Uhlenbeck (OU) hypothesis tests in lsquoouchrsquo for extrinsic (EHP) and intrinsic (IHP) hand proportions For each model we report a measure of relative model fit (ǻAICc) and support (Akaike weight9) The lowest ǻAICc score (0 in each case indicated in bold) represents the best-fit model Sensitivity analyses for EHP were iterated with a large (ArdiL 508 kg) and small (ArdiS 357 kg) body mass estimate for Ar ramidus as well as by excluding Ar ramidus and Proconsul heseloni (NO-Ardi-Pro) and Pr heseloni and all hylobatid species (NO-Pro-hylo) from the analysis

Model AICc ǻAICc AICc weightEHP ArdiL Brownian 32579 4114 000

OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000

OU5 lsquosurfacersquo 28464 000 100 OU5 lsquoaltrsquo 29951 1487 000

EHP ArdiS Brownian 32824 4359 000 OU1 33281 4816 000 OU2 32936 4472 000 OU4 31923 3459 000


EHP NO-Ardi-Pro Brownian 30522 3957 000 OU1 31461 4896 000 OU2 31178 4613 000 OU4 29413 2849 000


EHP NO-Pro-hylo Brownian 24887 3646 000 OU1 25239 3998 000 OU2 25688 4447 000 OU4 24574 3333 000


IHP Brownian -6898 5685 000 OU1 -7186 5397 000 OU2 -7252 5331 000 OU4 -9650 2932 000

OU5 lsquoEHPrsquo -8224 4359 000 OU3 lsquoIHP alt1rsquo -11479 1104 000

OU4 lsquoIHPrsquo -12583 000 100 OU4 lsquoIHP alt2rsquo -10896 1687 000

See Supplementary Figures 5 6 9 for descriptions of each model

ͳͻ

Supplementary Note 1 What is ldquopad-to-padrdquo precision grasping Among the vast array of grips that the human and ape hand are capable of Napier10 defined the term ldquoprecision griprdquo to describe instances in which the object being manipulated (with precision) was held between the palmar aspects of the fingers and the opposing thumb In contrast ldquopower griprdquo refers to situations in which the object is held in a ldquoclamp fashionrdquo between the flexed fingers and the palm and the thumb only plays a subsidiary role by directing the force being applied (as when using a hammer) The term ldquohuman-like precision graspingrdquo is commonly used in the literature although sometimes misunderstood chimpanzees and orangutans can efficiently manipulate objects via different forms of precision grasping (eg thumb and index finger tip-to-tip and pad-to-side)11112 However the characteristic human ldquopad-to-padrdquo precision grip (ie flat contact between the proximal pulps of the thumb and one or more fingers)13 is precluded in modern apes due to the disproportionate length of their digits II-V relative to the thumb1111415 (Fig 1) as well as by restricted passive hyperextension of the distal phalanges1215

With the exception of hylobatids a group that constitutes the exception to many rules in hand morphology1617 a clear trend is revealed within each anthropoid lineage the more arboreal species exhibit functionally shorter thumbs relative to the fingers As an example within extant great apes the highly arboreal orangutans followed by chimpanzees display relatively shorter thumbs than the more terrestrial gorillas which exhibit more generalized proportions (Fig 1) This has been related to the capability of performing an effective ldquohook grasprdquo during below-branch suspension11116 Among catarrhines only Theropithecus gelada approaches the human condition in terms of IHP as computed in our analysis (Fig 1) but since geladas exhibit an extremely shortened index finger18 this ldquoopposability indexrdquo would surpass the human condition if the index finger was the denominator instead of the fourth ray The IHP in this species are explained as a specific feeding adaptation in primates that spend 70 of their daily activity collecting food (blades of grass seeds and rhizomes) using precision grips19 The special adaptation of the hands of geladas is also evident in a special differentiation of the flexor digitorium profundus as well as other thumb muscles20 which is also reflected in their pollical distal phalanx morphology17 Capuchins (Cebus) monkeys are the only non-hominoid primates known to use tools habitually21 Although platyrrhines lack a ldquotrue opposable thumbrdquo11 capuchins (unlike other New World primates) commonly display both precision and power grips to manipulate objects such as use of stones as nut cracking tools and stone flakes as cutting tools22-24 Thus these behaviours are consistent with our results of intrinsic hand proportions (Fig1) which we find to be convergent with humans (Supplementary Fig 9)

ʹͲ

Supplementary Note 2 Evolutionary scenarios supported by the results of this work

Our results show that contrarily to the idea assumed by some extant great apes constitute a heterogeneous group in terms of hand and thumb proportions (Figs 1-2 Supplementary Figs 1-3) Furthermore our evolutionary modelling unambiguously shows that the chimpanzee-human LCA exhibited a moderate hand length (relative to overall body size) more similar to humans than to chimpanzees (Figs 3-4) Of special relevance is the fact that even using different phylogenetic hypotheses (Figs 5-6 Supplementary Figs 6-7) our results indicate that digital elongation has been achieved to different degrees and independently in the different extant and fossil ape lineages Although the evidence presented here is restricted to the hand broader implications can be reasonably drawn in terms of human and ape evolution

1 - Mosaicism and Parallelism in Ape Evolution

Together with previous analyses of limb proportions25 and skull morphology26 these results falsify the view that extant apes and particularly African apes constitute a homogeneous group with subtle deviations from a common allometric pattern27 Furthermore the degree of heterogeneity in hand proportions revealed here is congruent with a mosaic evolution of the hominoid postcranial skeleton as inferred before from the fossil record28-34 Our results indicating parallel evolution for digital elongation (with Pan and Pongo sharing convergent similarities Fig 3) match previous observations in other anatomical regions of modern apes35-40 In general the current evidence reinforces the view that specialized arboreal adaptations exhibited by the living apes are not identical because they evolved independently as biomechanical solutions to largely similar but far from identical positional and locomotor behaviours162935 and parallelism was facilitated by their common genetic and developmental base3741 One of the consequences of this hypothesis is that no extant ape will properly represent a living analogue for a given hypothetical ancestor2942

2 - Extant Hominoids Are Survivors

As pointed out before extant apes represent a very decimated expression of a highly diversified group during the Miocene4042-44 What explains their decay And why there are no fossil apes showing all the derived features of the living lineages A possible explanation is that offered by Pilbeam and colleagues45-47 who argue that we have not yet found any bona fide crown great ape in the fossil record Another hypothesis that we favour is that a select few hominoid lineages (living representatives) survived because they were adapted to specialized lifestyles eg enhanced antipronogrady and frugivory in hylobatids orangutans and chimpanzees large body size and folivory in gorillas and finally bipedalism and novel manual foraging strategies in hominins144849 and were able to compete with the radiation of the more generalized cercopithecids starting in the late Miocene4150 If that were the

ʹͳ

case it is striking that the European late Miocene HispanopithecusRudapithecus lineage (Fig 5) with clearly specialized suspensory adaptations in the hand and other anatomical regions28303451 became extinct at the end of the Miocene It seems that in this case the specialized lifestyle that allowed the survival of most extant ape lineages became an evolutionary trap for Hispanopithecus during to the ldquoVallesian crisisrdquo (ca 95 Ma) which caused its extinction mdashas well as that of other forest-adapted faunamdash as a consequence of paleoenvironmental changes associated with increased aridification and seasonality that caused the demise of the warm temperate forests (and year-round availability of fruit) in Western and Central Europe5253 Furthermore the results of this work indicate that suspensory behaviours in Hispanopithecus laietanus (as indicated by finger lengthening) evolved independently from other ape lineages (Fig 6) reinforcing the view that the West European Miocene apes constituted an independent evolutionary radiation

3 - Implications for Knuckle Walking

Humeral length relative to body mass is surprisingly similar in African apes and modern humans54 but it is relatively longer in orangutans and lesser apes These latter two suspensory hominoids also possess higher brachial indices (ie 100 x radius lengthhumerus length) whereas modern humans and gorillas have the lowest brachial indices among extant hominoids Proconsul Ardipithecus and australopiths (Au afarensis Au garhi and Au sediba) all have intermediate brachial indices that overlap with chimpanzees55 suggesting this to be the plesiomorphic proportionality for the upper limb of the African ape-human last common ancestor (LCA) However our results on extrinsic hand proportions (EHP) favour the hypothesis that gorillas and early hominins are the most conservative in terms of overall hand shape (Figs 3-4) in agreement with previous observations of Schultz56 This has implications for understanding the evolution of knuckle walking Classically the hands of great apes were seen as anatomical ldquohooksrdquo designed for below-branch suspension so they would be forced when on the ground to walk on the dorsal surfaces of their hooked hands3656 However this locomotor behaviour is currently seen as a compromise solution between the biomechanical requirements of advanced climbing and terrestrial digitigrady mdashrequiring long versus short fingers respectively5758 Based on the terrestrial fist-walking of orangutans Tuttle interpreted it as an intermediate stage between advanced arboreal suspension and terrestrial locomotion155859 Whereas fist-walking allowed the hand to be used as a supporting structure knuckle walking would further allow the manual phalanges to act as a propulsive lever during terrestrial quadrupedalism58 In our analyses (Fig 4) the EHP of the African ape LCA are reconstructed as moderate in digital length (ie most similar to the chimpanzee-human LCA) Thus irrespective of whether knuckle walking evolved only once at the base of the African ape lineage455760 or independently in gorillas and chimpanzees555861-63 our results imply that it was not related causally to the possession of especially long digits like those present in Pan or Pongo Contrarily

ʹʹ

origins of knuckle walking should probably be interpreted only in the light of an adaptive complex that would reduce the compressive stresses as well as the torques generated by the ground reaction force during hyperextension of the metacarpophalangeal joints during terrestrial quadrupedalism while still preserving a powerful grasping hand6465 Among other bony features it would be associated with short phalanges relative to metacarpals high dorsopalmar diameter of the metacarpal heads as well as pronounced dorsal ridges and large epicondyles on the metacarpal heads The question remains that if knuckle walking is such an efficient form of terrestrial quadrupedalism why has it not evolved in other primates too (as it has outside primates)66 The answer to this question is no doubt very complex ldquoregularrdquo (monkey-like) digitigrady might be restricted by a certain threshold of absolute digital length and body mass within an ancestral terrestrial setting Evolution of knuckle-walking was probably facilitated in African apes instead by their arboreal heritage15 having short tendons for the extrinsic flexor muscles is one of several limiting factors121567 and we hypothesize that the possession of an orthograde body plan as well as long forelimbs relative to hindlimbs combine to dictate the unusual way in which African apes can perform quadrupedalism

4 - Implications for Early Hominin Locomotion

In relation to the longstanding debate on the climbing capabilities of early hominins68-

71 our results mdashshowing similar digital length in gorillas and modern humans (Figs 2 4 Supplementary Fig 1)mdash imply that in terms of digital length there is no reason to think that climbing behaviours observed in gorillas72 were precluded in australopithecines In fact trained modern humans are excellent climbers73 even exceeding gorillas in acrobatic capabilities74 Relevant to the origins of bipedalism the preserved portions of the thorax and hand of the fossil great ape Pierolapithecusindicate that the acquisition of an orthograde body plan can be decoupled from specialized climbing and suspensory adaptations29 This evidence opens the possibility of human bipedalism having originated as a direct exaptation of arboreal orthogrady without an intermediate stage of advanced suspension or specialized knuckle walking

5 - Origins of the Human Hand

In terms of modern human hand proportions most of the evolutionary change is concentrated in digital elongationreduction (specifically metacarpal and proximal phalanx) whereas the thumb itself has remained more conservative with just slight thumb elongation in humans (especially via proximal pollical phalanx Supplementary Table 7) Therefore within living apes (and anthropoids) modern humans do not exhibit the shortest hands nor the longest thumbs but rather a useful combination that has been selected to allow enhanced thumb to fingers opposition (Fig 1) as it is revealed by our convergence results with Theropithecus and Cebus (Supplementary

ʹ͵

Fig 9) Furthermore these optimal intrinsic proportions evolved from a moderate ratio as inferred for the chimpanzee-human LCA estimation with less shape change than by assuming a chimpanzee-like LCA (Fig 4 Supplementary Fig 8) This confirms previous hypotheses based on observations of extant taxa fossil apes and early hominins17316375 and favors classic views of human evolution that preceded the molecular resolution of hominid phylogeny15566776-78 This and previous works indicate that enhanced thumb-to-digits opposition was present in australopiths sensulato144979-84 but see Rolian and Gordon for a different opinion on Au afarensis8586 This would not be the case of the early Pliocene (44 Ma) Ar ramidus that exhibits a shorter thumb relative to fingers (ie IHP in the gorilla and hylobatid range but longer than chimpanzees Fig 1) However evidence from the pollical distal phalanx morphology suggests that intrinsic hand proportions (IHP) similar to those of Australopithecushumans (allowing for enhanced ldquopad-to-padrdquo opposition) could be already present in the late Miocene (ca 6 Ma) Orrorin tugenensis4887 a hominin that was at least an incipient biped based on femoral morphology4088-92 Since both extrinsic (Fig 4) and intrinsic (Supplementary Fig 8) hand proportions in Ar ramidus seem largely plesiomorphic (for the African ape and human clade) this evidence suggests that although more recent in time than O tugenensis Ar ramidus more closely reflects the hand proportions of the chimpanzee-human LCA63 If this were the case this could represent a very early case of cladogenesis in the hominin lineage in which Ar ramidus would be more plesiomorphic than O tugenensis A possible explanation for this would be niche partitioning in early hominins with Ar ramidus being more committed to arboreal life than O tugenensis Short thumbs relative to digits have almost always been related to arboreal locomotion165693 an environment for which Ar ramidus was well suited in many other respects639495 More fossils of O tugenensis representing anatomies preserved in Ar ramidus would be necessary to test this hypothesis

A long thumb relative to fingers (ie high IHP Fig 1) facilitates enhanced pad-to-pad opposition and advanced manipulative skills in humans1 and other non-hominoid primates181922-24 But did this high human IHP ratio evolve specifically for stone tool making There is archaeological evidence indicating that stone tool use was part of the chimpanzee-human LCA behavioural repertoire2196 and thus not surprisingly also of Au afarensis97 Furthermore the thumb of O tugenensis suggests human-like IHP at 6 Ma disassociated of stone tools48 We hypothesize that both human-like IHP and stone tool using behaviours evolved prior to the widespread appearance of systematic stone tool making around 25 Ma9899 probably when the derived manual traits distinctive of modern humans and Neandertals first evolved100101 More recently the newly-described lithic artifacts from Lomekwi 3 (West Turkana Kenya) push back the earliest evidence of intentional stone tool production at 33 Ma102 which is consistent with human-like manual dexterity being an ancient adaptation amongst hominins Harmand et al argue that the decisive adaptation enabling ldquoLomekwianrdquo stone knapping most likely related to a reorganization of the central nervous system in

ʹͶ

yet unidentified hominins102

Thus among the many features characterizing the human hand11011 such as a high IHP would not have necessarily evolved originally as a specific adaptation to stone tool making Instead they probably evolved as a new foragingfeeding adaptive complex in the context of habitual bipedalism144874103 The relevance of bipedalism for the emergence of advanced manipulative skills in humans has been recognized ever since Darwin104 but also in more recent works1474105106 These authors share the same basic idea regular bipedalism allowed some degree of relaxation of the locomotor selective pressures acting in the upper extremity facilitating the manipulative selective pressures already present in all primates1 to refine hand length proportions for advanced manipulative tasks However although foot-hand coevolution could have occurred via shared developmental pathways (ie pleiotropic effects)107 our results indicate that these changes were relatively subtle (human manual hand proportions evolved from moderate mdashplesiomorphicmdash proportions not from a chimp-like ancestor Fig 4 and Supplementary Fig 8) Finally we agree with idea that human hand length proportions are largely plesiomorphic for the hominin clade and it was not until later in time when these proportions were co-opted108 for purposive and systematic stone tool making in hominins with more advanced cognitive capabilities144849102109

ʹͷ

Supplementary References

1 Napier J Hands [Revised by Russell H Tuttle] 180 (Princeton University Press 1993)

2 Revell L J Two new graphical methods for mapping trait evolution on phylogenies Methods Ecol Evol 4 754-759 (2013)

3 Felsenstein J Phylogenies and quantitative characters Annu Rev Ecol Syst 19 445-471 (1988)

4 Schluter D Price T Mooers A Oslash amp Ludwig D Likelihood of ancestor states in adaptive radiation Evolution 51 1699-1711 (1997)

5 Cavalli-Sforza L L amp Edwards A W Phylogenetic analysis Models and estimation procedures Am J Hum Genet 19 233 (1967)

6 Felsenstein J Maximum-likelihood estimation of evolutionary trees from continuous characters Am J Hum Genet 25 471 (1973)

7 Felsenstein J Phylogenies and the comparative method Am Nat 125 1-15 (1985)

8 Ingram T amp Mahler D L SURFACE detecting convergent evolution from comparative data by fitting Ornstein Uhlenbeck models with stepwise Akaike Information Criterion Methods Ecol Evol 4 416-425 (2013)

9 Burnham K P amp Anderson D R Model Selection and Multimodel Inference A Practical Information-theoretic Approach (Springer-Verlag 2002)

10 Napier J R The prehensile movements of the human hand J Bone Joint Surg Am 38 B 902-913 (1956)

11 Napier J R Studies of the hands of living primates Proc Zool Soc Lond 134 647-657 (1960)

12 Christel M in Hands of primates (eds Holger Preuschoft amp David J Chivers) 91-108 (Springer 1993)

13 Shrewsbury M M Marzke M W Linscheid R L amp Reece S P Comparative morphology of the pollical distal phalanx Am J Phys Anthropol 121 30-47 (2003)

14 Alba D M Moyagrave-Solagrave S amp Koumlhler M Morphological affinities of the Australopithecus afarensis hand on the basis of manual proportions and relative thumb length J Hum Evol 44 225-254 (2003)

15 Tuttle R H Knuckle-walking and the evolution of hominoid hands Am J Phys Anthropol 26 171-206 (1967)

16 Straus W L Jr Rudimentary digits in primates Q Rev Biol 17 228-243 (1942)

17 Almeacutecija S Shrewsbury M Rook L amp Moyagrave-Solagrave S The morphology of Oreopithecus bambolii pollical distal phalanx Am J Phys Anthropol 153 582-597 (2014)

18 Etter H F Terrestrial adaptations in the hands of Cercopithecinae Folia Primatol 20 331-350 (1973)

19 Jolly C J in Diverse Approaches in Human Evolution Vol 4 323-332 (1970)

20 Maier W Vergleichende und funktionell-anatomische Untersuchungen an der Vorderextremitaet von Theropithecus gelada (Rueppell 1835) AbhSenckenb naturforsch Ges 527 1-284 (1971)

ʹ

21 Panger M A Brooks A S Richmond B G amp Wood B Older than the Oldowan Rethinking the emergence of hominin tool use Evol Anthropol 11 235-245 (2002)

22 Costello M B amp Fragaszy D M Prehension in Cebus and Saimiri I Grip type and hand preference Am J Primatol 15 235-245 (1988)

23 Westergaard G C amp Suomi S J Capuchin monkey (Cebus apella) grips for the use of stone tools Am J Phys Anthropol 103 131-135 (1997)

24 Marzke M W Tool making hand morphology and fossil hominins Philos T Roy Soc B 368 20120414 (2013)

25 Jungers W L amp Hartman S E in Orang-utan Biology (ed Jeffrey H Schwartz) 347-359 (Oxford University Press 1988)

26 Mitteroecker P Gunz P Bernhard M Schaefer K amp Bookstein F L Comparison of cranial ontogenetic trajectories among great apes and humans J Hum Evol 46 679-698 (2004)

27 Shea B T Allometry and heterochrony in the African apes Am J Phys Anthropol 62 275-289 (1983)

28 Moyagrave-Solagrave S amp Koumlhler M A Dryopithecus skeleton and the origins of great-ape locomotion Nature 379 156-159 (1996)

29 Moyagrave-Solagrave S Koumlhler M Alba D M Casanovas-Vilar I amp Galindo J Pierolapithecus catalaunicus a new Middle Miocene great ape from Spain Science 306 1339-1344 (2004)

30 Almeacutecija S Alba D M Moyagrave-Solagrave S amp Koumlhler M Orang-like manual adaptations in the fossil hominoid Hispanopithecus laietanus first steps towards great ape suspensory behaviours P Roy Soc B 274 2375-2384 (2007)

31 Almeacutecija S Alba D M amp Moyagrave-Solagrave S Pierolapithecus and the functional morphology of Miocene ape hand phalanges paleobiological and evolutionary implications J Hum Evol 57 284-297 (2009)

32 Hammond A S Alba D M Almeacutecija S amp Moyagrave-Solagrave S Middle MiocenePierolapithecus provides a first glimpse into early hominid pelvic morphology J Hum Evol 64 658-666 (2013)

33 Tallman M Almeacutecija S Reber S L Alba D M amp Moyagrave-Solagrave S The distal tibia of Hispanopithecus laietanus More evidence for mosaic evolution in Miocene apes J Hum Evol 64 319-327 (2013)

34 Susanna I Alba D M Almeacutecija S amp Moyagrave-Solagrave S The vertebral remains of the late Miocene great ape Hispanopithecus laietanus from Can Llobateres 2 (Vallegraves-Penedegraves Basin NE Iberian Peninsula) J Hum Evol 73 15-34 (2014)

35 Larson S G Parallel evolution in the hominoid trunk and forelimb Evol Anthropol 6 87-99 (1998)

36 Erikson G E Brachiation in New World monkeys and in anthropoid apes Symp Zool Soc Lond 10 135-163 (1963)

37 Tuttle R in Phylogeny of the Primates (eds W Patrick Luckett amp Frederick S Szalay) 447-480 (Springer 1975)

38 Ward C in Handbook of Paleoanthropology (eds W Henke amp I Tattersall) 1011-1030 (Springer Verlag 2007)

39 Kivell T Barros A amp Smaers J Different evolutionary pathways underlie the morphology of wrist bones in hominoids BMC Evol Biol 13 229 (2013)

ʹ

40 Almeacutecija S et al The femur of Orrorin tugenensis exhibits morphometric affinities with both Miocene apes and later hominins Nat Commun 4 2888 (2013)

41 Reno P L Genetic and developmental basis for parallel evolution and its significance for hominoid evolution Evol Anthropol 23 188-200 (2014)

42 Harrison T The implications of Oreopithecus bambolii for the origins of bipedalism Origine(s) de la bipeacutedie chez les hominideacutes 235-244 (1991)

43 Alba D M Fossil apes from the Vallegraves-Penedegraves Basin Evol Anthropol 21 254-269 (2012)

44 Begun D R Nargolwalla M C amp Kordos L European Miocene hominids and the origin of the African ape and human clade Evol Anthropol 21 10-23 (2012)

45 Pilbeam D amp Young N Hominoid evolution synthesizing disparate data CR Palevol 3 305-321 (2004)

46 Pilbeam D R Rose M D Barry J C amp Shah S M I New Sivapithecushumeri from Pakistan and the relationship of Sivapithecus and Pongo Nature 348 237-239 (1990)

47 Morgan M E et al A partial hominoid innominate from the Miocene of Pakistan Description and preliminary analyses P Natl Acad Sci USA Early Edition (2014)

48 Almeacutecija S Moyagrave-Solagrave S amp Alba D M Early origin for human-like precision grasping A comparative study of pollical distal phalanges in fossil hominins PLoS ONE 5 e11727 (2010)

49 Almeacutecija S amp Alba D M On manual proportions and pad-to-pad precision grasping in Australopithecus afarensis J Hum Evol 73 88-92 (2014)

50 Jablonski N G Whitfort M J Roberts-Smith N amp Qinqi X The influence of life history and diet on the distribution of catarrhine primates during the Pleistocene in eastern Asia J Hum Evol 39 131-157 (2000)

51 Pina M Alba D M Almeacutecija S Fortuny J amp Moyagrave-Solagrave S Brief communication Paleobiological inferences on the locomotor repertoire of extinct hominoids based on femoral neck cortical thickness The fossil great ape Hispanopithecus laietanus as a test-case study Am J Phys Anthropol 149 142-148 (2012)

52 DeMiguel D Alba D M amp Moyagrave-Solagrave S Dietary specialization during the evolution of Western Eurasian hominoids and the extinction of European great apes PLoS ONE 9 e97442 (2014)

53 Casanovas-Vilar I Alba D M Garceacutes M Robles J M amp Moyagrave-Solagrave S Updated chronology for the Miocene hominoid radiation in Western Eurasia P Natl Acad Sci USA 108 5554-5559 (2011)

54 Jungers W L Ape and hominid limb length Nature 369 194-194 (1994) 55 Lovejoy C O Suwa G Simpson S W Matternes J H amp White T D

The great divides Ardipithecus ramidus reveals the postcrania of our last common ancestors with African apes Science 326 73-106 (2009)

56 Schultz A H The skeleton of the trunk and limbs of higher primates HumBiol 2 303-438 (1930)

57 Richmond B G Begun D R amp Strait D S Origin of human bipedalism the knuckle-walking hypothesis revisited Yearb Phys Anthropol 44 70-105 (2001)

58 Tuttle R H Knuckle-walking and the problem of human origins Science 166 953-961 (1969)

ʹͺ

59 Tuttle R Knuckle walking hand postures in an orangutan (Pongo pygmaeus) Nature 236 33-34 (1972)

60 Williams S A Morphological integration and the evolution of knuckle-walking J Hum Evol 58 432-440 (2010)

61 Dainton M amp Macho G A Did knuckle walking evolve twice J Hum Evol 36 171-194 (1999)

62 Kivell T L amp Schmitt D Independent evolution of knuckle-walking in African apes shows that humans did not evolve from a knuckle-walking ancestor P Natl Acad Sci USA Early Edition (2009)

63 Lovejoy C O Simpson S W White T D Asfaw B amp Suwa G Careful climbing in the Miocene The forelimbs of Ardipithecus ramidus and humans are primitive Science 326 70-708 (2009)

64 Preuschoft H Functional anatomy of the upper extremity The Chimpanzee 6 34-120 (1973)

65 Susman R L Comparative and functional morphology of hominoid fingers Am J Phys Anthropol 50 215-236 (1979)

66 Orr C M Knuckle-walking anteater A convergence test of adaption for purported knuckle-walking features of African Hominidae Am J Phys Anthropol (2005)

67 Straus W L Jr The posture of the great ape hand in locomotion and its phylogenetic implications Am J Phys Anthropol 27 199-207 (1940)

68 Johanson D C et al Morphology of the Pliocene partial hominid skeleton (AL 288-1) from the Hadar Formation Ethiopia Am J Phys Anthropol 57 403-451 (1982)

69 Stern J T Jr amp Susman R L The locomotor anatomy of Australopithecus afarensis Am J Phys Anthropol 60 279-317 (1983)

70 Stern J T J Climbing to the top a personal memoir of Australopithecus afarensis Evol Anthropol 9 113-133 (2000)

71 Ward C V Kimbel W H amp Johanson D C Complete fourth metatarsal and arches in the foot of Australopithecus afarensis Science 331 750-753 (2011)

72 Remis M Effects of body size and social context on the arboreal activities of lowland gorillas in the Central African Republic Am J Phys Anthropol 97 413-433 (1995)

73 Venkataraman V V Kraft T S amp Dominy N J Tree climbing and human evolution P Natl Acad Sci USA (2012)

74 Hewes G W Food transport and the origin of hominid bipedalism Am Anthropol 63 687-710 (1961)

75 Almeacutecija S Alba D M amp Moyagrave-Solagrave S The thumb of Miocene apes New insights from Castell de Barberagrave (Catalonia Spain) Am J Phys Anthropol 148 436-450 (2012)

76 Straus W L Jr The riddle of mans ancestry Q Rev Biol 24 200-223 (1949)

77 Schultz A H Characters common to higher primates and characters specific for man Q Rev Biol 11 259-283 (1936)

78 Le Gros Clark W E The Fossil Evidence for Human Evolution 200 (University of Chicago Press 1964)

79 Kivell T L Kibii J M Churchill S E Schmid P amp Berger L R Australopithecus sediba hand demonstrates mosaic evolution of locomotor and manipulative abilities Science 333 1411-1417 (2011)

ʹͻ

80 Green D J amp Gordon A Metacarpal proportions in Australopithecus africanus J Hum Evol 54 705-719 (2008)

81 Marzke M W Joint functions and grips of the Australopithecus afarensis hand with special reference to the region of capitate J Hum Evol 12 197-211 (1983)

82 Susman R L Hand of Paranthopus robustus from member 1 Swartkrans Fossil evidence for tool behavior Science 240 781-784 (1988)

83 Susman R L Fossil evidence for early hominid tool use Science 265 1570-1573 (1994)

84 Skinner M M et al Human-like hand use in Australopithecus africanus Science 347 395-399 (2015)

85 Rolian C amp Gordon A D Reassessing manual proportions in Australopithecus afarensis Am J Phys Anthropol 152 393-406 (2013)

86 Rolian C amp Gordon A D Response to Almeacutecija and Alba (2014) ndash On manual proportions in Australopithecus afarensis J Hum Evol 73 93-97 (2014)

87 Gommery D amp Senut B La phalange distale du pouce dOrrorin tugenensis (Miocegravene supeacuterieur du Kenya) Geobios 39 372-284 (2006)

88 Pickford M Senut B Gommery D amp Treil J Bipedalism in Orrorintugenensis revealed by its femora C R Palevol 1 191-203 (2002)

89 Galik K et al External and internal morphology of the BAR 100200 Orrorintugenensis femur Science 305 1450-1453 (2004)

90 Richmond B G amp Jungers W L Orrorin tugenensis femoral morphology and the evolution of hominin bipedalism Science 319 1662-1665 (2008)

91 Richmond B G amp Jungers W L in African Genesis Perspectives on Hominin Evolution (eds Sally C Reynolds amp Andrew Gallagher) 248-267 (Cambridge University Press 2012)

92 Senut B Pickford M Gommery D amp Kunimatsu Y Un nouveau genge dhominoiumlde du Miocegravene infeacuterieur dAfrique orientale Ugandapithecus major (Le Gros Clark amp Leakey 1950) C R Acad Sci Paris 331 227-233 (2000)

93 Ashley-Montagu F M On the primate thumb Am J Phys Anthropol 25 291-314 (1931)

94 White T D et al Ardipithecus ramidus and the paleobiology of early hominids Science 326 64-86 (2009)

95 Lovejoy C O Latimer B Suwa G Asfaw B amp White T D Combining prehension and propulsion The foot of Ardipithecus ramidus Science 326 72-728 (2009)

96 Mercader J Panger M amp Boesch C Excavation of a chimpanzee stone tool site in the African rainforest Science 296 1452-1455 (2002)

97 McPherron S P et al Evidence for stone-tool-assisted consumption of animal tissues before 339 million years ago at Dikika Ethiopia Nature 466 857-860 (2010)

98 Semaw S et al 25-million-year-old stone tools from Gona Ethiopia Nature 385 333-336 (1997)

99 Semaw S et al 26-Million-year-old stone tools and associated bones from OGS-6 and OGS-7 Gona Afar Ethiopia J Hum Evol 45 169-177 (2003)

100 Tocheri M W Orr C M Jacofsky M C amp Marzke M W The evolutionary history of the hominin hand since the last common ancestor of Pan and Homo J Anat 212 544-562 (2008)

͵Ͳ

101 Ward C V Tocheri M W Plavcan J M Brown F H amp Manthi F K Early Pleistocene third metacarpal from Kenya and the evolution of modern human-like hand morphology P Natl Acad Sci USA 111 121-124 (2014)

102 Harmand S et al 33-million-year-old stone tools from Lomekwi 3 West Turkana Kenya Nature 521 310-315 (2015)

103 Hunt K D The postural feeding hypothesis An ecological model for the evolution of bipedalism S Afr J Sci 92 77 (1996)

104 Darwin C The Descent of Man and Selection in Relation to Sex (John Murray 1871)

105 Hartwig W C amp Doneski K Evolution of the hominid hand and tool making behavior Am J Phys Anthropol 106 401-402 (1998)

106 Jouffroy F K in Origine(s) de la Bipeacutedie Chez les Hominideacutes (eds B Senut amp Y Coppens) 21-35 (Editions du CNRS 1991)

107 Rolian C Lieberman D E amp Hallgriacutemsson B The coevolution of human hands and feet Evolution 64 1558-1568 (2010)

108 Gould S J amp Vrba E S Exaptation-a missing term in the science of form Paleobiology 8 4-15 (1982)

109 Napier J Fossil hand bones from Olduvai Gorge Nature 196 409-411 (1962)

title_link

Figuretrade1Intrinsic hand proportions of humans and other anthropoid primates(a) Drawings of a chimpanzee and human hands are shown to similar scale (b) Relative length of the thumb=pollicalsolfourth ray lengths (minus distal fourth phalanx see inset) Bo

Results

Intrinsic hand proportions

Extrinsic hand proportions

Figuretrade2Extrinsic hand proportions of humans and other anthropoid primates(a) Principal components analysis of the body mass-adjusted hand lengths (b) Summary of the contribution of each hand element in selected anthropoids Species are arranged by maxi

The evolution of human and ape hand proportions

Figuretrade3Time-calibrated phylogenetic tree showing the estimated adaptive regimes in our anthropoid sampleAdaptive optima are based on the two major axes of extrinsic hand proportions (EHP) variation between extant and fossil species (accounting for 945p

Figuretrade4The evolutionary history of human and ape hand proportionsPhylomorphospace projection of the phylogeny presented in Figtrade3 onto the two first principal components (PCs) of extrinsic hand proportions (EHP) in extant and fossil species Taxa are co

Figuretrade5The hand of the late Miocene ape Hispanopithecus laietanusIts reconstructed hand is displayed in dorsal (a) and palmar (b) views and together with its associated skeleton (c) This species represents the earliest specialized adaptations for belo

Discussion

Methods


Figuretrade6Reconstructed evolutionary histories of human and ape digital extrinsic proportionsThe phylomorphospace approach was limited to the three long bones of ray IV to include the fossil ape Hispanopithecus laietanus and Ateles species The same analys

Shape analyses of extrinsic hand proportions

Allometric regressions

Body mass estimation

Phylogenetic trees

Multi-regime OU modelling

Phylomorphospace

Phylogenetic signal

NapierJHands180Princeton Univ Press1993LovejoyC OSimpsonS WWhiteT DAsfawBSuwaGCareful climbing in the Miocene The forelimbs of Ardipithecus ramidus and humans are primitiveScience326707082009TuttleRinPhylogeny of the PrimatesedsLuckettW Patr

We are indebted to the following researchers and curators for granting access to collections under their care Emma Mbua National Museum of Kenya Salvador Moyagrave-Solagrave Institut Catalagrave de Paleontologia Miquel Crusafont Yoel Rak Tel Aviv University Emman

ACKNOWLEDGEMENTS

Author contributions

Additional information

The hand is one of the most distinctive traits of humankindand one of our main sources of interaction with theenvironment1 The human hand can be distinguished

from that of apes by its long thumb relative to fingers1ndash4 (Fig 1a)which has been related functionally to different selectiveregimesmdashmanipulation vs locomotionmdashacting on human andape hands15 During the first half of the twentieth centurytheories on human evolution were dominated by the view thathumans split very early from the common stock of apes andlargely preserved generalized (plesiomorphic) hand proportionssimilar to other anthropoid primates6ndash8 To the contrary extantapes were seen as extremely specialized animals adapted forbelow-branch suspension67 However since the molecularrevolution in the 1980ndash1990s (which provided unequivocalevidence for humans and chimpanzees being sister taxa)9 aprevalent and influential evolutionary paradigmmdashsaid to be basedon parsimonymdashhas assumed that the last common ancestor(LCA) of chimpanzees and humans was similar to a modernchimpanzee (for example ref 10) This shift resurrected thelsquotroglodytianrsquo stage in human evolution which assumes that achimp-like knuckle-walking ancestor preceded human bipedalism(for example ref 11) Most subsequent hypotheses dealing withhuman hand evolution have been framed assuming a lsquolong-handedshort-thumbedrsquo chimp-like hand as the starting points ofthe LCA and basal hominins with strong selective pressuresacting to reverse these proportions in the context of stone tool-making andor as a by-product of drastic changes in footmorphology in the human career (for example ref 12) Howeverthe current fossil evidence of early hominins251314 and fossil

apes15ndash18 challenges this paradigm Collectively these fossilssuggest instead that hand proportions approaching the modernhuman condition could in fact be largely plesiomorphic2413 aswas previously suggested before the advent of molecularphylogenetics If that were the case this would have profoundimplications relevant to the locomotor adaptations of thechimpanzee-human LCA as well as the relationship betweenhuman hand structure and the origins of systematized stone toolculture

To address this complex discussion and to provide a deeperunderstanding on the evolution of the human and ape hand inthis study we perform a stepwise series of detailed morphometricand evolutionary analyses on the hand-length proportions ofmodern apes and humans as compared with a large sample ofextant anthropoid primates and key fossils preserving sufficientlycomplete associated hands This fossil sample is constituted bythe early hominins Ardipithecus ramidus (44 Myr ago)2 andAustralopithecus sediba (B2 Myr ago)14 as well as the primitiveAfrican ape Proconsul heseloni (B18 Myr ago)15 and the Europeanfossil great ape Hispanopithecus laietanus (96 Myr ago)17 First weinspect thumb length relative to the lateral digits (as revealed byray four that is intrinsic hand proportions) to show thathumans are distinctive from apes for this important functionalmeasure but not from some other anthropoids Second weanalyse individual hand elements as proportions adjusted viaoverall body size (that is extrinsic hand proportions) to testwhether modern apesmdashand more especially African greatapesmdashrepresent a homogeneous group from which humansdepart Here we further show that modern hominoids constitute

AlouattaCebus

NasalisMacaca

MandrillusPapio

TheropithecusHylobatidae

Po pygmaeusPo abeliiG gorilla

G beringeiPa paniscus

Pa troglodytesHo sapiens

ARA-VP-6500Ar ramidus

Pr heseloniKebara 2

Ho neanderthalensis

MH2Au sediba

Qafzeh 9early Ho sapiens

Relative thumb length (intrinsic)085075065055045035

Chimpanzee Human

a b Modern humansModern apes

Figure 1 | Intrinsic hand proportions of humans and other anthropoid primates (a) Drawings of a chimpanzee and human hands are shown to similarscale (b) Relative length of the thumbfrac14 pollicalfourth ray lengths (minus distal fourth phalanx see inset) Box represents the interquartile rangecenterline is the median whiskers represent non-outlier range and dots are outliers The ranges of humans and modern apes are highlighted (green andred-shaded areas respectively) Samples for each boxplot are Homo sapiens (nfrac1440) Pan troglodytes (nfrac14 34) Pan paniscus (nfrac14 12) Gorilla beringei (nfrac14 21)Gorilla gorilla (nfrac14 13) Pongo abelii (nfrac148) Pongo pygmaeus (nfrac14 19) Hylobatidae (nfrac14 14) Theropithecus (nfrac14 5) Papio (nfrac14 50) Mandrillus (nfrac14 3) Macaca(nfrac14 18) Nasalis (nfrac14 14) Cebus (nfrac14 11) and Alouatta (nfrac14 8) The values for Pr heseloni and Ar ramidus are projected onto the remaining taxa to facilitatevisual comparisons









ndash20ndash1000

1020

30

20

10

00

ndash10


10

20

30

40

50

60

70

80

Pollicalmetacarpal


Fourthmetacarpal




Rel

ativ

e le

ngth

Po pygmaeus

Hy lar

G beringei

Pa troglodytes

Ho sapiens

ARA-VP-6500

Ar ramidus S

Pr heseloni

Al seniculus

ARA-VP-6500

Ar ramidus L

T geladaPC 3 (669)

PC

2 (

104

8)

PC 1 (7977)

Theropithecus


Papio


NasalisMacaca

Hylobatidae

Ho sapiens

G beringeiG gorilla

CebusAlouatta

Qafzeh 9

Kebara 2MH 2


Pr heseloni

a b

Mandrillus









Proconsul heseloni


Hylobates agilis






Hom

inoidea

40 30 20 10 0Myr

Hylobatidae

Hom

inidaeC

ercopithecidae

Platyrrhini

Catarrhini







minus10 minus5 0 5 10 15 20

minus50

5

PC 1 (8621)

PC

2 (

830

)

b

Ar ramidus

Ar ramidus

minus10 minus5 0 5 10 15 20

ndash50

5

PC 1 (8634)

PC

2 (

818

)



N larvatus


T gelada

Pap hamadryas

Pr heseloni

S syndactylus

Hy pileatus

Hy lar




Pa troglodytes

Ho sapiens

Honeanderthalensis

Au sediba

Root

a

Great ape-human LCA

Chimpanzee-humanLCA

(+ 95 CI)


0

10

20

30

40

50

60Relative length

Pa troglodytes

Ho sapiens

Chimpanzee-

human LCA


Chimpanzee-

human LCA

0

10

20

30

40

50

60

Pa troglodytes

Ho sapiens

Relative length

c

d














50





40 30 20 10 0





50 40 30 20 10 0





50 40 30 20 10 0

d e f

a b c

Myr MyrMyr











minus10 minus5 0 5 10 15 20

minus5

0

5

PC 1 (9283)

PC

2 (

688

)



N larvatus


T gelada

Pap hamadryas


Hy lar

Hy agilis

Hy moloch

Hy muelleri


G gorillaG beringei

Pa paniscus

Pa troglodytes

Ar ramidus

Honeanderthalensis

Au sediba

minus10 minus5 0 5 10 15 20

minus5

0

5

PC 1 (9275)

PC

2 (

696

)



Pr heseloni



a

Ar ramidus

Great ape-human LCA


Root









































































































ͳ


ʹ


͵


Ͷ


ͷ



7

minus10 minus5 0 5 10 15 20

minus50

5

PC 1 (8651)

PC 2

(82

6)



N larvatus



S syndactylus

Hy pileatus

Hy lar




Pa troglodytes

Ho sapiens

Honeanderthalensis

Au sediba

great ape-human LCA

chimpanzee-humanLCA

(+ 95 CI)

Root


ͺ


ͻ


ͳͲ


ͳͳ







ͳʹ










ͳ͵



Pa troglodytes 1000

G gorilla 0031 0000

G beringei 0000 0000 1000

Po abelii 0000 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0208 0000 1000 1000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0000 0000 0000 0000 0012 0000 0000

Mandrillus 0000 0000 0000 0001 0000 0000 0000 0000 1000 0000

Macaca 0000 0000 0002 0269 0000 0000 0000 0000 0597 0000 0520

Nasalis 0516 1000 0000 0000 0123 0000 0000 0000 0000 0000 0000 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 1000 0000 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0008 0000 1000 0000 0000 0000


ͳͶ






ͳͷ



Pa troglodytes 1000

G gorilla 0005 0000

G beringei 0000 0000 1000

Po abelii 0005 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0000 0000 0000 0000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0004 0000 0000 0000 0000 0000 0000

Mandrillus 0043 0000 0508 0002 0007 0000 0001 0005 0004 1000

Macaca 0000 0000 0018 0000 0000 0000 0000 0000 0000 0000 0234

Nasalis 0001 0000 0001 0000 0001 0000 0000 0000 0000 0000 0002 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0002 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0001 0000 0000 0000


ͳ






ͳ






ͳͺ



OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000












ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS








ndash20ndash1000

1020

30

20

10

00

ndash10


10

20

30

40

50

60

70

80

Pollicalmetacarpal


Fourthmetacarpal




Rel

ativ

e le

ngth

Po pygmaeus

Hy lar

G beringei

Pa troglodytes

Ho sapiens

ARA-VP-6500

Ar ramidus S

Pr heseloni

Al seniculus

ARA-VP-6500

Ar ramidus L

T geladaPC 3 (669)

PC

2 (

104

8)

PC 1 (7977)

Theropithecus


Papio


NasalisMacaca

Hylobatidae

Ho sapiens

G beringeiG gorilla

CebusAlouatta

Qafzeh 9

Kebara 2MH 2


Pr heseloni

a b

Mandrillus









Proconsul heseloni


Hylobates agilis






Hom

inoidea

40 30 20 10 0Myr

Hylobatidae

Hom

inidaeC

ercopithecidae

Platyrrhini

Catarrhini







minus10 minus5 0 5 10 15 20

minus50

5

PC 1 (8621)

PC

2 (

830

)

b

Ar ramidus

Ar ramidus

minus10 minus5 0 5 10 15 20

ndash50

5

PC 1 (8634)

PC

2 (

818

)



N larvatus


T gelada

Pap hamadryas

Pr heseloni

S syndactylus

Hy pileatus

Hy lar




Pa troglodytes

Ho sapiens

Honeanderthalensis

Au sediba

Root

a

Great ape-human LCA

Chimpanzee-humanLCA

(+ 95 CI)


0

10

20

30

40

50

60Relative length

Pa troglodytes

Ho sapiens

Chimpanzee-

human LCA


Chimpanzee-

human LCA

0

10

20

30

40

50

60

Pa troglodytes

Ho sapiens

Relative length

c

d














50





40 30 20 10 0





50 40 30 20 10 0





50 40 30 20 10 0

d e f

a b c

Myr MyrMyr











minus10 minus5 0 5 10 15 20

minus5

0

5

PC 1 (9283)

PC

2 (

688

)



N larvatus


T gelada

Pap hamadryas


Hy lar

Hy agilis

Hy moloch

Hy muelleri


G gorillaG beringei

Pa paniscus

Pa troglodytes

Ar ramidus

Honeanderthalensis

Au sediba

minus10 minus5 0 5 10 15 20

minus5

0

5

PC 1 (9275)

PC

2 (

696

)



Pr heseloni



a

Ar ramidus

Great ape-human LCA


Root









































































































ͳ


ʹ


͵


Ͷ


ͷ



7

minus10 minus5 0 5 10 15 20

minus50

5

PC 1 (8651)

PC 2

(82

6)



N larvatus



S syndactylus

Hy pileatus

Hy lar




Pa troglodytes

Ho sapiens

Honeanderthalensis

Au sediba

great ape-human LCA

chimpanzee-humanLCA

(+ 95 CI)

Root


ͺ


ͻ


ͳͲ


ͳͳ







ͳʹ










ͳ͵



Pa troglodytes 1000

G gorilla 0031 0000

G beringei 0000 0000 1000

Po abelii 0000 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0208 0000 1000 1000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0000 0000 0000 0000 0012 0000 0000

Mandrillus 0000 0000 0000 0001 0000 0000 0000 0000 1000 0000

Macaca 0000 0000 0002 0269 0000 0000 0000 0000 0597 0000 0520

Nasalis 0516 1000 0000 0000 0123 0000 0000 0000 0000 0000 0000 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 1000 0000 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0008 0000 1000 0000 0000 0000


ͳͶ






ͳͷ



Pa troglodytes 1000

G gorilla 0005 0000

G beringei 0000 0000 1000

Po abelii 0005 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0000 0000 0000 0000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0004 0000 0000 0000 0000 0000 0000

Mandrillus 0043 0000 0508 0002 0007 0000 0001 0005 0004 1000

Macaca 0000 0000 0018 0000 0000 0000 0000 0000 0000 0000 0234

Nasalis 0001 0000 0001 0000 0001 0000 0000 0000 0000 0000 0002 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0002 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0001 0000 0000 0000


ͳ






ͳ






ͳͺ



OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000












ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS







Proconsul heseloni


Hylobates agilis






Hom

inoidea

40 30 20 10 0Myr

Hylobatidae

Hom

inidaeC

ercopithecidae

Platyrrhini

Catarrhini







minus10 minus5 0 5 10 15 20

minus50

5

PC 1 (8621)

PC

2 (

830

)

b

Ar ramidus

Ar ramidus

minus10 minus5 0 5 10 15 20

ndash50

5

PC 1 (8634)

PC

2 (

818

)



N larvatus


T gelada

Pap hamadryas

Pr heseloni

S syndactylus

Hy pileatus

Hy lar




Pa troglodytes

Ho sapiens

Honeanderthalensis

Au sediba

Root

a

Great ape-human LCA

Chimpanzee-humanLCA

(+ 95 CI)


0

10

20

30

40

50

60Relative length

Pa troglodytes

Ho sapiens

Chimpanzee-

human LCA


Chimpanzee-

human LCA

0

10

20

30

40

50

60

Pa troglodytes

Ho sapiens

Relative length

c

d














50





40 30 20 10 0





50 40 30 20 10 0





50 40 30 20 10 0

d e f

a b c

Myr MyrMyr











minus10 minus5 0 5 10 15 20

minus5

0

5

PC 1 (9283)

PC

2 (

688

)



N larvatus


T gelada

Pap hamadryas


Hy lar

Hy agilis

Hy moloch

Hy muelleri


G gorillaG beringei

Pa paniscus

Pa troglodytes

Ar ramidus

Honeanderthalensis

Au sediba

minus10 minus5 0 5 10 15 20

minus5

0

5

PC 1 (9275)

PC

2 (

696

)



Pr heseloni



a

Ar ramidus

Great ape-human LCA


Root









































































































ͳ


ʹ


͵


Ͷ


ͷ



7

minus10 minus5 0 5 10 15 20

minus50

5

PC 1 (8651)

PC 2

(82

6)



N larvatus



S syndactylus

Hy pileatus

Hy lar




Pa troglodytes

Ho sapiens

Honeanderthalensis

Au sediba

great ape-human LCA

chimpanzee-humanLCA

(+ 95 CI)

Root


ͺ


ͻ


ͳͲ


ͳͳ







ͳʹ










ͳ͵



Pa troglodytes 1000

G gorilla 0031 0000

G beringei 0000 0000 1000

Po abelii 0000 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0208 0000 1000 1000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0000 0000 0000 0000 0012 0000 0000

Mandrillus 0000 0000 0000 0001 0000 0000 0000 0000 1000 0000

Macaca 0000 0000 0002 0269 0000 0000 0000 0000 0597 0000 0520

Nasalis 0516 1000 0000 0000 0123 0000 0000 0000 0000 0000 0000 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 1000 0000 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0008 0000 1000 0000 0000 0000


ͳͶ






ͳͷ



Pa troglodytes 1000

G gorilla 0005 0000

G beringei 0000 0000 1000

Po abelii 0005 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0000 0000 0000 0000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0004 0000 0000 0000 0000 0000 0000

Mandrillus 0043 0000 0508 0002 0007 0000 0001 0005 0004 1000

Macaca 0000 0000 0018 0000 0000 0000 0000 0000 0000 0000 0234

Nasalis 0001 0000 0001 0000 0001 0000 0000 0000 0000 0000 0002 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0002 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0001 0000 0000 0000


ͳ






ͳ






ͳͺ



OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000












ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS





minus10 minus5 0 5 10 15 20

minus50

5

PC 1 (8621)

PC

2 (

830

)

b

Ar ramidus

Ar ramidus

minus10 minus5 0 5 10 15 20

ndash50

5

PC 1 (8634)

PC

2 (

818

)



N larvatus


T gelada

Pap hamadryas

Pr heseloni

S syndactylus

Hy pileatus

Hy lar




Pa troglodytes

Ho sapiens

Honeanderthalensis

Au sediba

Root

a

Great ape-human LCA

Chimpanzee-humanLCA

(+ 95 CI)


0

10

20

30

40

50

60Relative length

Pa troglodytes

Ho sapiens

Chimpanzee-

human LCA


Chimpanzee-

human LCA

0

10

20

30

40

50

60

Pa troglodytes

Ho sapiens

Relative length

c

d














50





40 30 20 10 0





50 40 30 20 10 0





50 40 30 20 10 0

d e f

a b c

Myr MyrMyr











minus10 minus5 0 5 10 15 20

minus5

0

5

PC 1 (9283)

PC

2 (

688

)



N larvatus


T gelada

Pap hamadryas


Hy lar

Hy agilis

Hy moloch

Hy muelleri


G gorillaG beringei

Pa paniscus

Pa troglodytes

Ar ramidus

Honeanderthalensis

Au sediba

minus10 minus5 0 5 10 15 20

minus5

0

5

PC 1 (9275)

PC

2 (

696

)



Pr heseloni



a

Ar ramidus

Great ape-human LCA


Root









































































































ͳ


ʹ


͵


Ͷ


ͷ



7

minus10 minus5 0 5 10 15 20

minus50

5

PC 1 (8651)

PC 2

(82

6)



N larvatus



S syndactylus

Hy pileatus

Hy lar




Pa troglodytes

Ho sapiens

Honeanderthalensis

Au sediba

great ape-human LCA

chimpanzee-humanLCA

(+ 95 CI)

Root


ͺ


ͻ


ͳͲ


ͳͳ







ͳʹ










ͳ͵



Pa troglodytes 1000

G gorilla 0031 0000

G beringei 0000 0000 1000

Po abelii 0000 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0208 0000 1000 1000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0000 0000 0000 0000 0012 0000 0000

Mandrillus 0000 0000 0000 0001 0000 0000 0000 0000 1000 0000

Macaca 0000 0000 0002 0269 0000 0000 0000 0000 0597 0000 0520

Nasalis 0516 1000 0000 0000 0123 0000 0000 0000 0000 0000 0000 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 1000 0000 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0008 0000 1000 0000 0000 0000


ͳͶ






ͳͷ



Pa troglodytes 1000

G gorilla 0005 0000

G beringei 0000 0000 1000

Po abelii 0005 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0000 0000 0000 0000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0004 0000 0000 0000 0000 0000 0000

Mandrillus 0043 0000 0508 0002 0007 0000 0001 0005 0004 1000

Macaca 0000 0000 0018 0000 0000 0000 0000 0000 0000 0000 0234

Nasalis 0001 0000 0001 0000 0001 0000 0000 0000 0000 0000 0002 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0002 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0001 0000 0000 0000


ͳ






ͳ






ͳͺ



OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000












ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS












50





40 30 20 10 0





50 40 30 20 10 0





50 40 30 20 10 0

d e f

a b c

Myr MyrMyr











minus10 minus5 0 5 10 15 20

minus5

0

5

PC 1 (9283)

PC

2 (

688

)



N larvatus


T gelada

Pap hamadryas


Hy lar

Hy agilis

Hy moloch

Hy muelleri


G gorillaG beringei

Pa paniscus

Pa troglodytes

Ar ramidus

Honeanderthalensis

Au sediba

minus10 minus5 0 5 10 15 20

minus5

0

5

PC 1 (9275)

PC

2 (

696

)



Pr heseloni



a

Ar ramidus

Great ape-human LCA


Root









































































































ͳ


ʹ


͵


Ͷ


ͷ



7

minus10 minus5 0 5 10 15 20

minus50

5

PC 1 (8651)

PC 2

(82

6)



N larvatus



S syndactylus

Hy pileatus

Hy lar




Pa troglodytes

Ho sapiens

Honeanderthalensis

Au sediba

great ape-human LCA

chimpanzee-humanLCA

(+ 95 CI)

Root


ͺ


ͻ


ͳͲ


ͳͳ







ͳʹ










ͳ͵



Pa troglodytes 1000

G gorilla 0031 0000

G beringei 0000 0000 1000

Po abelii 0000 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0208 0000 1000 1000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0000 0000 0000 0000 0012 0000 0000

Mandrillus 0000 0000 0000 0001 0000 0000 0000 0000 1000 0000

Macaca 0000 0000 0002 0269 0000 0000 0000 0000 0597 0000 0520

Nasalis 0516 1000 0000 0000 0123 0000 0000 0000 0000 0000 0000 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 1000 0000 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0008 0000 1000 0000 0000 0000


ͳͶ






ͳͷ



Pa troglodytes 1000

G gorilla 0005 0000

G beringei 0000 0000 1000

Po abelii 0005 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0000 0000 0000 0000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0004 0000 0000 0000 0000 0000 0000

Mandrillus 0043 0000 0508 0002 0007 0000 0001 0005 0004 1000

Macaca 0000 0000 0018 0000 0000 0000 0000 0000 0000 0000 0234

Nasalis 0001 0000 0001 0000 0001 0000 0000 0000 0000 0000 0002 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0002 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0001 0000 0000 0000


ͳ






ͳ






ͳͺ



OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000












ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS









minus10 minus5 0 5 10 15 20

minus5

0

5

PC 1 (9283)

PC

2 (

688

)



N larvatus


T gelada

Pap hamadryas


Hy lar

Hy agilis

Hy moloch

Hy muelleri


G gorillaG beringei

Pa paniscus

Pa troglodytes

Ar ramidus

Honeanderthalensis

Au sediba

minus10 minus5 0 5 10 15 20

minus5

0

5

PC 1 (9275)

PC

2 (

696

)



Pr heseloni



a

Ar ramidus

Great ape-human LCA


Root









































































































ͳ


ʹ


͵


Ͷ


ͷ



7

minus10 minus5 0 5 10 15 20

minus50

5

PC 1 (8651)

PC 2

(82

6)



N larvatus



S syndactylus

Hy pileatus

Hy lar




Pa troglodytes

Ho sapiens

Honeanderthalensis

Au sediba

great ape-human LCA

chimpanzee-humanLCA

(+ 95 CI)

Root


ͺ


ͻ


ͳͲ


ͳͳ







ͳʹ










ͳ͵



Pa troglodytes 1000

G gorilla 0031 0000

G beringei 0000 0000 1000

Po abelii 0000 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0208 0000 1000 1000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0000 0000 0000 0000 0012 0000 0000

Mandrillus 0000 0000 0000 0001 0000 0000 0000 0000 1000 0000

Macaca 0000 0000 0002 0269 0000 0000 0000 0000 0597 0000 0520

Nasalis 0516 1000 0000 0000 0123 0000 0000 0000 0000 0000 0000 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 1000 0000 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0008 0000 1000 0000 0000 0000


ͳͶ






ͳͷ



Pa troglodytes 1000

G gorilla 0005 0000

G beringei 0000 0000 1000

Po abelii 0005 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0000 0000 0000 0000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0004 0000 0000 0000 0000 0000 0000

Mandrillus 0043 0000 0508 0002 0007 0000 0001 0005 0004 1000

Macaca 0000 0000 0018 0000 0000 0000 0000 0000 0000 0000 0234

Nasalis 0001 0000 0001 0000 0001 0000 0000 0000 0000 0000 0002 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0002 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0001 0000 0000 0000


ͳ






ͳ






ͳͺ



OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000












ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS







































































































ͳ


ʹ


͵


Ͷ


ͷ



7

minus10 minus5 0 5 10 15 20

minus50

5

PC 1 (8651)

PC 2

(82

6)



N larvatus



S syndactylus

Hy pileatus

Hy lar




Pa troglodytes

Ho sapiens

Honeanderthalensis

Au sediba

great ape-human LCA

chimpanzee-humanLCA

(+ 95 CI)

Root


ͺ


ͻ


ͳͲ


ͳͳ







ͳʹ










ͳ͵



Pa troglodytes 1000

G gorilla 0031 0000

G beringei 0000 0000 1000

Po abelii 0000 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0208 0000 1000 1000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0000 0000 0000 0000 0012 0000 0000

Mandrillus 0000 0000 0000 0001 0000 0000 0000 0000 1000 0000

Macaca 0000 0000 0002 0269 0000 0000 0000 0000 0597 0000 0520

Nasalis 0516 1000 0000 0000 0123 0000 0000 0000 0000 0000 0000 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 1000 0000 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0008 0000 1000 0000 0000 0000


ͳͶ






ͳͷ



Pa troglodytes 1000

G gorilla 0005 0000

G beringei 0000 0000 1000

Po abelii 0005 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0000 0000 0000 0000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0004 0000 0000 0000 0000 0000 0000

Mandrillus 0043 0000 0508 0002 0007 0000 0001 0005 0004 1000

Macaca 0000 0000 0018 0000 0000 0000 0000 0000 0000 0000 0234

Nasalis 0001 0000 0001 0000 0001 0000 0000 0000 0000 0000 0002 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0002 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0001 0000 0000 0000


ͳ






ͳ






ͳͺ



OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000












ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ʹ


͵


Ͷ


ͷ



7

minus10 minus5 0 5 10 15 20

minus50

5

PC 1 (8651)

PC 2

(82

6)



N larvatus



S syndactylus

Hy pileatus

Hy lar




Pa troglodytes

Ho sapiens

Honeanderthalensis

Au sediba

great ape-human LCA

chimpanzee-humanLCA

(+ 95 CI)

Root


ͺ


ͻ


ͳͲ


ͳͳ







ͳʹ










ͳ͵



Pa troglodytes 1000

G gorilla 0031 0000

G beringei 0000 0000 1000

Po abelii 0000 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0208 0000 1000 1000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0000 0000 0000 0000 0012 0000 0000

Mandrillus 0000 0000 0000 0001 0000 0000 0000 0000 1000 0000

Macaca 0000 0000 0002 0269 0000 0000 0000 0000 0597 0000 0520

Nasalis 0516 1000 0000 0000 0123 0000 0000 0000 0000 0000 0000 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 1000 0000 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0008 0000 1000 0000 0000 0000


ͳͶ






ͳͷ



Pa troglodytes 1000

G gorilla 0005 0000

G beringei 0000 0000 1000

Po abelii 0005 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0000 0000 0000 0000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0004 0000 0000 0000 0000 0000 0000

Mandrillus 0043 0000 0508 0002 0007 0000 0001 0005 0004 1000

Macaca 0000 0000 0018 0000 0000 0000 0000 0000 0000 0000 0234

Nasalis 0001 0000 0001 0000 0001 0000 0000 0000 0000 0000 0002 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0002 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0001 0000 0000 0000


ͳ






ͳ






ͳͺ



OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000












ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



͵


Ͷ


ͷ



7

minus10 minus5 0 5 10 15 20

minus50

5

PC 1 (8651)

PC 2

(82

6)



N larvatus



S syndactylus

Hy pileatus

Hy lar




Pa troglodytes

Ho sapiens

Honeanderthalensis

Au sediba

great ape-human LCA

chimpanzee-humanLCA

(+ 95 CI)

Root


ͺ


ͻ


ͳͲ


ͳͳ







ͳʹ










ͳ͵



Pa troglodytes 1000

G gorilla 0031 0000

G beringei 0000 0000 1000

Po abelii 0000 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0208 0000 1000 1000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0000 0000 0000 0000 0012 0000 0000

Mandrillus 0000 0000 0000 0001 0000 0000 0000 0000 1000 0000

Macaca 0000 0000 0002 0269 0000 0000 0000 0000 0597 0000 0520

Nasalis 0516 1000 0000 0000 0123 0000 0000 0000 0000 0000 0000 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 1000 0000 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0008 0000 1000 0000 0000 0000


ͳͶ






ͳͷ



Pa troglodytes 1000

G gorilla 0005 0000

G beringei 0000 0000 1000

Po abelii 0005 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0000 0000 0000 0000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0004 0000 0000 0000 0000 0000 0000

Mandrillus 0043 0000 0508 0002 0007 0000 0001 0005 0004 1000

Macaca 0000 0000 0018 0000 0000 0000 0000 0000 0000 0000 0234

Nasalis 0001 0000 0001 0000 0001 0000 0000 0000 0000 0000 0002 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0002 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0001 0000 0000 0000


ͳ






ͳ






ͳͺ



OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000












ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



Ͷ


ͷ



7

minus10 minus5 0 5 10 15 20

minus50

5

PC 1 (8651)

PC 2

(82

6)



N larvatus



S syndactylus

Hy pileatus

Hy lar




Pa troglodytes

Ho sapiens

Honeanderthalensis

Au sediba

great ape-human LCA

chimpanzee-humanLCA

(+ 95 CI)

Root


ͺ


ͻ


ͳͲ


ͳͳ







ͳʹ










ͳ͵



Pa troglodytes 1000

G gorilla 0031 0000

G beringei 0000 0000 1000

Po abelii 0000 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0208 0000 1000 1000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0000 0000 0000 0000 0012 0000 0000

Mandrillus 0000 0000 0000 0001 0000 0000 0000 0000 1000 0000

Macaca 0000 0000 0002 0269 0000 0000 0000 0000 0597 0000 0520

Nasalis 0516 1000 0000 0000 0123 0000 0000 0000 0000 0000 0000 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 1000 0000 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0008 0000 1000 0000 0000 0000


ͳͶ






ͳͷ



Pa troglodytes 1000

G gorilla 0005 0000

G beringei 0000 0000 1000

Po abelii 0005 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0000 0000 0000 0000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0004 0000 0000 0000 0000 0000 0000

Mandrillus 0043 0000 0508 0002 0007 0000 0001 0005 0004 1000

Macaca 0000 0000 0018 0000 0000 0000 0000 0000 0000 0000 0234

Nasalis 0001 0000 0001 0000 0001 0000 0000 0000 0000 0000 0002 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0002 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0001 0000 0000 0000


ͳ






ͳ






ͳͺ



OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000












ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ͷ



7

minus10 minus5 0 5 10 15 20

minus50

5

PC 1 (8651)

PC 2

(82

6)



N larvatus



S syndactylus

Hy pileatus

Hy lar




Pa troglodytes

Ho sapiens

Honeanderthalensis

Au sediba

great ape-human LCA

chimpanzee-humanLCA

(+ 95 CI)

Root


ͺ


ͻ


ͳͲ


ͳͳ







ͳʹ










ͳ͵



Pa troglodytes 1000

G gorilla 0031 0000

G beringei 0000 0000 1000

Po abelii 0000 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0208 0000 1000 1000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0000 0000 0000 0000 0012 0000 0000

Mandrillus 0000 0000 0000 0001 0000 0000 0000 0000 1000 0000

Macaca 0000 0000 0002 0269 0000 0000 0000 0000 0597 0000 0520

Nasalis 0516 1000 0000 0000 0123 0000 0000 0000 0000 0000 0000 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 1000 0000 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0008 0000 1000 0000 0000 0000


ͳͶ






ͳͷ



Pa troglodytes 1000

G gorilla 0005 0000

G beringei 0000 0000 1000

Po abelii 0005 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0000 0000 0000 0000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0004 0000 0000 0000 0000 0000 0000

Mandrillus 0043 0000 0508 0002 0007 0000 0001 0005 0004 1000

Macaca 0000 0000 0018 0000 0000 0000 0000 0000 0000 0000 0234

Nasalis 0001 0000 0001 0000 0001 0000 0000 0000 0000 0000 0002 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0002 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0001 0000 0000 0000


ͳ






ͳ






ͳͺ



OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000












ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS




7

minus10 minus5 0 5 10 15 20

minus50

5

PC 1 (8651)

PC 2

(82

6)



N larvatus



S syndactylus

Hy pileatus

Hy lar




Pa troglodytes

Ho sapiens

Honeanderthalensis

Au sediba

great ape-human LCA

chimpanzee-humanLCA

(+ 95 CI)

Root


ͺ


ͻ


ͳͲ


ͳͳ







ͳʹ










ͳ͵



Pa troglodytes 1000

G gorilla 0031 0000

G beringei 0000 0000 1000

Po abelii 0000 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0208 0000 1000 1000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0000 0000 0000 0000 0012 0000 0000

Mandrillus 0000 0000 0000 0001 0000 0000 0000 0000 1000 0000

Macaca 0000 0000 0002 0269 0000 0000 0000 0000 0597 0000 0520

Nasalis 0516 1000 0000 0000 0123 0000 0000 0000 0000 0000 0000 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 1000 0000 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0008 0000 1000 0000 0000 0000


ͳͶ






ͳͷ



Pa troglodytes 1000

G gorilla 0005 0000

G beringei 0000 0000 1000

Po abelii 0005 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0000 0000 0000 0000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0004 0000 0000 0000 0000 0000 0000

Mandrillus 0043 0000 0508 0002 0007 0000 0001 0005 0004 1000

Macaca 0000 0000 0018 0000 0000 0000 0000 0000 0000 0000 0234

Nasalis 0001 0000 0001 0000 0001 0000 0000 0000 0000 0000 0002 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0002 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0001 0000 0000 0000


ͳ






ͳ






ͳͺ



OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000












ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ͺ


ͻ


ͳͲ


ͳͳ







ͳʹ










ͳ͵



Pa troglodytes 1000

G gorilla 0031 0000

G beringei 0000 0000 1000

Po abelii 0000 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0208 0000 1000 1000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0000 0000 0000 0000 0012 0000 0000

Mandrillus 0000 0000 0000 0001 0000 0000 0000 0000 1000 0000

Macaca 0000 0000 0002 0269 0000 0000 0000 0000 0597 0000 0520

Nasalis 0516 1000 0000 0000 0123 0000 0000 0000 0000 0000 0000 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 1000 0000 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0008 0000 1000 0000 0000 0000


ͳͶ






ͳͷ



Pa troglodytes 1000

G gorilla 0005 0000

G beringei 0000 0000 1000

Po abelii 0005 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0000 0000 0000 0000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0004 0000 0000 0000 0000 0000 0000

Mandrillus 0043 0000 0508 0002 0007 0000 0001 0005 0004 1000

Macaca 0000 0000 0018 0000 0000 0000 0000 0000 0000 0000 0234

Nasalis 0001 0000 0001 0000 0001 0000 0000 0000 0000 0000 0002 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0002 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0001 0000 0000 0000


ͳ






ͳ






ͳͺ



OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000












ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ͻ


ͳͲ


ͳͳ







ͳʹ










ͳ͵



Pa troglodytes 1000

G gorilla 0031 0000

G beringei 0000 0000 1000

Po abelii 0000 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0208 0000 1000 1000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0000 0000 0000 0000 0012 0000 0000

Mandrillus 0000 0000 0000 0001 0000 0000 0000 0000 1000 0000

Macaca 0000 0000 0002 0269 0000 0000 0000 0000 0597 0000 0520

Nasalis 0516 1000 0000 0000 0123 0000 0000 0000 0000 0000 0000 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 1000 0000 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0008 0000 1000 0000 0000 0000


ͳͶ






ͳͷ



Pa troglodytes 1000

G gorilla 0005 0000

G beringei 0000 0000 1000

Po abelii 0005 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0000 0000 0000 0000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0004 0000 0000 0000 0000 0000 0000

Mandrillus 0043 0000 0508 0002 0007 0000 0001 0005 0004 1000

Macaca 0000 0000 0018 0000 0000 0000 0000 0000 0000 0000 0234

Nasalis 0001 0000 0001 0000 0001 0000 0000 0000 0000 0000 0002 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0002 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0001 0000 0000 0000


ͳ






ͳ






ͳͺ



OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000












ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ͳͲ


ͳͳ







ͳʹ










ͳ͵



Pa troglodytes 1000

G gorilla 0031 0000

G beringei 0000 0000 1000

Po abelii 0000 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0208 0000 1000 1000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0000 0000 0000 0000 0012 0000 0000

Mandrillus 0000 0000 0000 0001 0000 0000 0000 0000 1000 0000

Macaca 0000 0000 0002 0269 0000 0000 0000 0000 0597 0000 0520

Nasalis 0516 1000 0000 0000 0123 0000 0000 0000 0000 0000 0000 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 1000 0000 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0008 0000 1000 0000 0000 0000


ͳͶ






ͳͷ



Pa troglodytes 1000

G gorilla 0005 0000

G beringei 0000 0000 1000

Po abelii 0005 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0000 0000 0000 0000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0004 0000 0000 0000 0000 0000 0000

Mandrillus 0043 0000 0508 0002 0007 0000 0001 0005 0004 1000

Macaca 0000 0000 0018 0000 0000 0000 0000 0000 0000 0000 0234

Nasalis 0001 0000 0001 0000 0001 0000 0000 0000 0000 0000 0002 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0002 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0001 0000 0000 0000


ͳ






ͳ






ͳͺ



OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000












ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ͳͳ







ͳʹ










ͳ͵



Pa troglodytes 1000

G gorilla 0031 0000

G beringei 0000 0000 1000

Po abelii 0000 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0208 0000 1000 1000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0000 0000 0000 0000 0012 0000 0000

Mandrillus 0000 0000 0000 0001 0000 0000 0000 0000 1000 0000

Macaca 0000 0000 0002 0269 0000 0000 0000 0000 0597 0000 0520

Nasalis 0516 1000 0000 0000 0123 0000 0000 0000 0000 0000 0000 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 1000 0000 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0008 0000 1000 0000 0000 0000


ͳͶ






ͳͷ



Pa troglodytes 1000

G gorilla 0005 0000

G beringei 0000 0000 1000

Po abelii 0005 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0000 0000 0000 0000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0004 0000 0000 0000 0000 0000 0000

Mandrillus 0043 0000 0508 0002 0007 0000 0001 0005 0004 1000

Macaca 0000 0000 0018 0000 0000 0000 0000 0000 0000 0000 0234

Nasalis 0001 0000 0001 0000 0001 0000 0000 0000 0000 0000 0002 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0002 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0001 0000 0000 0000


ͳ






ͳ






ͳͺ



OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000












ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ͳʹ










ͳ͵



Pa troglodytes 1000

G gorilla 0031 0000

G beringei 0000 0000 1000

Po abelii 0000 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0208 0000 1000 1000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0000 0000 0000 0000 0012 0000 0000

Mandrillus 0000 0000 0000 0001 0000 0000 0000 0000 1000 0000

Macaca 0000 0000 0002 0269 0000 0000 0000 0000 0597 0000 0520

Nasalis 0516 1000 0000 0000 0123 0000 0000 0000 0000 0000 0000 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 1000 0000 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0008 0000 1000 0000 0000 0000


ͳͶ






ͳͷ



Pa troglodytes 1000

G gorilla 0005 0000

G beringei 0000 0000 1000

Po abelii 0005 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0000 0000 0000 0000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0004 0000 0000 0000 0000 0000 0000

Mandrillus 0043 0000 0508 0002 0007 0000 0001 0005 0004 1000

Macaca 0000 0000 0018 0000 0000 0000 0000 0000 0000 0000 0234

Nasalis 0001 0000 0001 0000 0001 0000 0000 0000 0000 0000 0002 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0002 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0001 0000 0000 0000


ͳ






ͳ






ͳͺ



OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000












ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ͳ͵



Pa troglodytes 1000

G gorilla 0031 0000

G beringei 0000 0000 1000

Po abelii 0000 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0208 0000 1000 1000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0000 0000 0000 0000 0012 0000 0000

Mandrillus 0000 0000 0000 0001 0000 0000 0000 0000 1000 0000

Macaca 0000 0000 0002 0269 0000 0000 0000 0000 0597 0000 0520

Nasalis 0516 1000 0000 0000 0123 0000 0000 0000 0000 0000 0000 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 1000 0000 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0008 0000 1000 0000 0000 0000


ͳͶ






ͳͷ



Pa troglodytes 1000

G gorilla 0005 0000

G beringei 0000 0000 1000

Po abelii 0005 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0000 0000 0000 0000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0004 0000 0000 0000 0000 0000 0000

Mandrillus 0043 0000 0508 0002 0007 0000 0001 0005 0004 1000

Macaca 0000 0000 0018 0000 0000 0000 0000 0000 0000 0000 0234

Nasalis 0001 0000 0001 0000 0001 0000 0000 0000 0000 0000 0002 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0002 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0001 0000 0000 0000


ͳ






ͳ






ͳͺ



OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000












ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ͳͶ






ͳͷ



Pa troglodytes 1000

G gorilla 0005 0000

G beringei 0000 0000 1000

Po abelii 0005 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0000 0000 0000 0000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0004 0000 0000 0000 0000 0000 0000

Mandrillus 0043 0000 0508 0002 0007 0000 0001 0005 0004 1000

Macaca 0000 0000 0018 0000 0000 0000 0000 0000 0000 0000 0234

Nasalis 0001 0000 0001 0000 0001 0000 0000 0000 0000 0000 0002 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0002 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0001 0000 0000 0000


ͳ






ͳ






ͳͺ



OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000












ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ͳͷ



Pa troglodytes 1000

G gorilla 0005 0000

G beringei 0000 0000 1000

Po abelii 0005 0000 0000 0000

Po pygmaeus 0000 0000 0000 0000 1000

Ho sapiens 0000 0000 0000 0000 0000 0000

Hylobatidae 0000 0000 0000 0000 0000 0000 0000

Papio 0000 0000 0000 0000 0000 0000 0000 0000

Theropithecus 0000 0000 0004 0000 0000 0000 0000 0000 0000

Mandrillus 0043 0000 0508 0002 0007 0000 0001 0005 0004 1000

Macaca 0000 0000 0018 0000 0000 0000 0000 0000 0000 0000 0234

Nasalis 0001 0000 0001 0000 0001 0000 0000 0000 0000 0000 0002 0000

Cebus 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0002 0000 0000

Alouatta 0000 0000 0000 0000 0000 0000 0000 0000 0000 0000 0001 0000 0000 0000


ͳ






ͳ






ͳͺ



OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000












ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ͳ






ͳ






ͳͺ



OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000












ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ͳ






ͳͺ



OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000












ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ͳͺ



OU1 32986 4521 000 OU2 32677 4213 000 OU4 31670 3206 000












ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ͳͻ



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ʹͲ







ʹͳ




ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ʹͳ




ʹʹ







ʹ͵



ʹͶ



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title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ʹʹ







ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ʹ͵



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ʹͶ



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ʹͷ






















ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ʹ




















ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ʹ




















ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ʹͺ






















ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



ʹͻ






















͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



͵Ͳ










title_link


Results








Discussion

Methods






Phylogenetic trees


Phylomorphospace

Phylogenetic signal



ACKNOWLEDGEMENTS



the evolution of human and ape hand proportions · the evolution of human and ape hand proportions...

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