reassessing manual proportions in australopithecus afarensis

Reassessing Manual Proportions in Australopithecusafarensis

Campbell Rolian1* and Adam D. Gordon2

1Department of Comparative Biology and Experimental Medicine, Faculty of Veterinary Medicine,University of Calgary, Calgary, Alberta, Canada T2N4N12Department of Anthropology, University at Albany—SUNY, Albany, NY 12222

KEY WORDS resampling methods; manual proportions; Australopithecus afarensis;Hadar formation; manipulative ability

ABSTRACT Previous analyses of hand morphologyin Australopithecus afarensis have concluded that thistaxon had modern human-like manual proportions, withrelatively long thumbs and short fingers. These conclu-sions are based on the A.L.333 composite fossil assem-blage from Hadar, Ethiopia, and are premised on theability to assign phalanges to a single individual, and tothe correct side and digit. Neither assignment is secure,however, given the taphonomy and sample compositionat A.L.333. We use a resampling approach that includesthe entire assemblage of complete hand elements atHadar, and takes into account uncertainties in identify-ing phalanges by individual, side and digit number. Thisapproach provides the most conservative estimates ofmanual proportions in Au. afarensis. We resampledhand long bone lengths in Au. afarensis and extant hom-

inoids, and obtained confidence limits for distributions ofmanual proportions in the latter. Results confirm thatintrinsic manual proportions in Au. afarensis are dissim-ilar to Pan and Pongo. However, manual proportions inAu. afarensis often fall at the upper end of the distributionin Gorilla, and very lower end in Homo, corresponding todisproportionately short thumbs and long medial digits inHomo. This suggests that manual proportions in Au. afar-ensis, particularly metacarpal proportions, were not asderived towards Homo as previously described, but ratherare intermediate between gorillas and humans. Function-ally, these results suggest Au. afarensis could not produceprecision grips with the same efficiency as modernhumans, which may in part account for the absence oflithic technology in this fossil taxon. Am J Phys Anthropol000:000–000, 2013. VC 2013 Wiley Periodicals, Inc.

Intrinsic hand proportions in extant hominoids havelong played an important role in assessing hand functionin fossil hominins (Napier, 1962; Susman et al., 1984;Marzke, 1997; Kivell et al., 2011). With respect tomanipulative ability, the length of the thumb relative tothe medial digits is seen as a key indicator of digit tip-to-tip opposability and precision grasping in homininhands, and by extension, of the potential ability to use andmanufacture tools (Napier and Tuttle, 1993; Tocheri et al.,2008). Associated hand remains from a single individualare rare in the hominin fossil record, however, making itdifficult to determine manual proportions with confidencefor most fossil taxa (but see Clarke, 1999; Kivell et al.,2011). This is especially true for fossil taxa from the mid-to late Pliocene (�4.0–2.5 million years ago), the timeperiod that immediately precedes the appearance of stonetools in the archaeological record (Semaw et al., 1997).

Previous accounts of manual proportions in the Plio-cene taxon Australopithecus afarensis have concludedthat its extrinsic and intrinsic hand proportions aremost similar to modern humans—characterized by a rel-atively long thumb and short medial digits (Marzke,1983; Alba et al., 2003). As there is yet no direct evi-dence of stone tool use or manufacture in Au. afarensis(although see McPherron et al., 2010, and subsequentdebate in the literature), such studies imply that thederived hand proportions in Au. afarensis and modernhumans did not evolve in the context of selection forenhanced precision grasping. However, no adult associ-ated/articulated hand remains have been recovered sofar in Au. afarensis. Previous reconstructions of manualproportions in Au. afarensis have in fact included either

small numbers of unassociated manual elements—mostunattributable to individual or even to digital ray(Marzke, 1983; Latimer, 1991)—or a composite handassumed to belong to a single individual (Alba et al.,2003). No study to date has included all known manualelements attributable to Au. afarensis. More impor-tantly, previous studies have also excluded larger pha-langeal elements from some fossil localities (e.g.,proximal phalanx A.L.333w-4, middle phalangesA.L.333x-18, and A.L.333-46), potentially biasing esti-mated manual proportions in this hominin. Here, we usea resampling method that provides the most

Additional Supporting Information may be found in the online ver-sion of this article.

Grant sponsor: National Science Foundation Doctoral Disserta-tion Improvement Grant; Grant number: BCS 0647624; Grant spon-sors: Natural Sciences and Engineering Research Council ofCanada; Faculty of Veterinary Medicine, University of Calgary (toCR); Wenner–Gren Hunt Postdoctoral Fellowship (to ADG).

*Correspondence to: Campbell Rolian, Department of Compara-tive Biology and Experimental Medicine, Faculty of Veterinary Med-icine, University of Calgary, 3330 Hospital Drive NW, Calgary,Alberta, Canada T2N4N1. E-mail: [email protected]

Received 25 April 2013; accepted 19 August 2013

DOI: 10.1002/ajpa.22365Published online 00 Month 2013 in Wiley Online Library

(wileyonlinelibrary.com).

� 2013 WILEY PERIODICALS, INC.

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 00:00–00 (2013)

conservative estimate of manual proportions in Au. afar-ensis. The method considers the consequences ofunknown taphonomic factors on fossil samples that maybias the estimation of manual proportions, including theinability to attribute disarticulated elements to ray orside and to determine with confidence the number ofindividuals represented in a fossil assemblage.

Hand material in Au. afarensis

All of our knowledge regarding digit morphology inAu. afarensis comes from the Pliocene fossil localities ofthe Afar region in Ethiopia (Kimbel and Delezene,2009). As this study focuses on manual length propor-tions, the Au. afarensis carpal material will not be con-sidered here (see Bush et al., 1982; Ward et al., 2012).Among the upper limb bones recovered in the Afar, threesites have yielded associated forelimb and hand longbones belonging to single individuals. The Dikika juve-nile specimen (DIK-1-1) includes three manual pha-langes, two of which are articulated, and a fragmentarydistal humerus (Alemseged et al., 2006). None of themanual phalanges appears to be pollical, precluding thecalculation of relative thumb length in this juvenilespecimen. A large individual with associated forelimb,hand and cranial remains, dated to �3.0 MY, was recov-ered at A.L. 438 (Drapeau et al., 2005: see below).The complete ulna and a few complete medial metacar-pals in A.L. 438-1d were used to estimate extrinsic pro-portions of the metacarpus relative to the forelimb(Drapeau et al., 2005). Finally, the partial skeleton A.L.288-1 (“Lucy”) includes a nearly complete humerus andradius, and a single, nonpollical, manual proximal pha-lanx that has not been attributed to a particular ray(Bush et al., 1982; Johanson et al., 1982a). Lucy’s fore-limb elements have been used to assess extrinsic phalan-geal proportions in Au. afarensis (Latimer, 1991: seebelow).

The best sample of hand long bones in Au. afarensiswas recovered at Hadar locality A.L. 333, the site of the“first family” (Johanson et al., 1980, 1982b). This sitealone accounts for over 90% of recovered Au. afarensismaterial (Ward et al., 2012). The assemblage containsover 200 fossils, and represents a minimum number of13 individuals, including 9 adults with considerablevariation in body size (Johanson et al., 1982b; Kimbeland Delezene, 2009). The original A.L. 333 hand mate-rial recovered in the 1970s include �20 complete longbones, including representatives from all metacarpalsand a pollical proximal phalanx, as well as fragmentaryremains from over 25 additional elements (Bush et al.,1982). Further discoveries from more recent field sea-sons at Hadar have added another �10 manual ele-ments for A.L. 333, including complete metacarpalsand phalanges (Ward et al., 2012). Finally, a few addi-tional hand long bones have been recovered in theAfar from sites other than the ones described above.These include complete proximal phalanges fromA.L. 444 and A.L. 1044-1, as well as fragmentaryremains from A.L. 724-3. All are described in Wardet al. (2012).

Previous assessments of manualproportions in Au. afarensis

Extrinsic proportions. There are no associated fore-limb elements in Au. afarensis that include all bonesfrom humerus to distal phalanx for any ray, and thus an

assessment of digital ray length relative to forearm andarm length is not possible in this taxon. Drapeau et al.(2005) used the associated ulna and medial metacarpalsin A.L. 438-1d to obtain an index of the length of themetacarpus relative to the forearm. Their analysis sug-gests that all hominoids, including Australopithecus,show similar length relationships between the medialmetacarpals and forearm, except for Pan, in which themedial metacarpals are thought to be autapomorphicallylong.

Latimer (1991) used the associated proximal phalanx,humerus and femur in A.L. 288-1 to suggest that pha-langeal length in Australopithecus was comparable tomodern humans, and unlike that of any extant ape. Lat-imer further argued that the apparent shortening of thefingers in A.L. 288-1 demonstrates that “the upper limbof Australopithecus afarensis had failed to maintainarboreal competence” (Latimer, 1991: p 174). It shouldbe noted, however, that Latimer’s analysis rests on theassumption that the proximal phalanx recovered forLucy (A.L. 288-1x) is a third proximal phalanx, whichhas never been conclusively demonstrated (Bush et al.,1982; Johanson et al., 1982). In the absence of clear mor-phological markers for identifying isolated medial pha-langes, there is an equal probability that this phalanxderives from a digit other than the third. In fact, if A.L.288-1x is assumed to come from any other digit, all ofwhich are shorter than the third digit in hominoids,then the length relationship between this phalanx andthe proximal limb bones becomes markedly different(Fig. 1).

Intrinsic proportions. Marzke (1983) used the A.L.333 hand sample and a small comparative sample ofchimpanzee and human hands to investigate relativethumb and third digit lengths in Au. afarensis. For thefossil sample, Marzke used the only complete thumbmetacarpal (A.L. 333w-39), proximal pollical phalanx(A.L. 333-69), and third metacarpal (A.L. 333-16) avail-able at the time, and the longest proximal and interme-diate phalanges from the A.L. 333 locality to representthe third digit. Marzke specifically excluded the signifi-cantly longer proximal phalanx from the nearby A.L.333w locality, A.L. 333w-4, on the grounds that it likelydid not come from the same individual as the other ele-ments (even though she used the first metacarpal fromA.L. 333w in her reconstruction). Marzke concluded thatrelative thumb length in Au. afarensis was significantlymore human-like than chimpanzee-like.

The most comprehensive analysis of manual propor-tions was published by Alba et al. (2003). Based on per-ceived size compatibility and joint congruence, Albaet al. (2003) reconstructed a composite hand from A.L.333 that includes all manual elements distal to the car-pus, except for the fourth intermediate phalanx and dis-tal phalanges (13 elements). Using a large comparativesample of extant great apes and humans, they per-formed discriminant analyses on the 13 elements toassess the morphological affinity of the composite Au.afarensis hand. The authors used raw length data, aswell as shape ratio and residual data adjusted for man-ual length (based on third ray) or body mass. To test therobustness of their results, Alba et al. (2003) also cre-ated 1,000 chimeric hands for each extant hominoid (i.e.,composite hands derived from more than one individual)and ran these through the discriminant analysis. Their

2 C. ROLIAN AND A.D. GORDON

American Journal of Physical Anthropology

results suggested that regardless of the type of dataused, the composite hand in Au. afarensis was most likeHomo, with a relative thumb length significantly closerto modern humans than to apes. Identical results wereobtained when chimeric extant hands were used, a factthat the authors used to argue that the inferred propor-tions in Au. afarensis are correct even if the fossil handis a composite. Alba et al. (2003) conclude that derivedproportions in Au. afarensis and Homo are mainly theresult of finger shortening (Latimer, 1991), rather thanthumb elongation.

The use of a randomization technique to create com-posite hominoid hands is a valid approach to address thelikelihood that the A.L. 333 hand is itself a reliable com-posite. Alba and colleagues’ randomization approach,however, did not allow the Au. afarensis hand itself tobe randomized. The full assemblage from A.L. 333/333wcontains more metacarpal and phalangeal elements thanare needed for a 13- or 14-variable hand reconstruction.Thus, there is more than one possible chimeric hand inthe Au. afarensis sample. For the phalangeal rays alone,the 6 complete medial proximal phalanges and 5 inter-mediate phalanges known in 2003 yield 75 unique com-binations of 4 proximal phalanges and 4 intermediatephalanges (because none can be reliably identified byindividual, ray or even side). Because Alba et al. (2003)opted to reconstruct a hand belonging to a single indi-vidual, many of these combinations can be excluded onthe basis of mismatched size relationships among digits.Crucially, as in Marzke’s (1983) analysis, their recon-struction excludes A.L. 333w-4, the longest proximalphalanx. Including additional combinations in discrimi-nant analyses, especially those that contain A.L. 333w-4,could potentially yield greater overlap in morphospacebetween Au. afarensis and chimeric hominoid hands.

Moreover, the composite hand in Alba et al. (2003) fur-ther assumes that the identity of the phalangeal ele-ments at A.L. 333 is known. As none of the elements atA.L. 333 was found associated or in anatomical connec-tion, the identity and side of the phalangeal elementscannot be ascertained on taphonomic grounds (Bushet al., 1982). Yet identifying elements by ray is necessaryin order to obtain shape ratios or residuals based on thelength of the third ray. Such ratios and residuals would

differ substantially if all available phalangeal elementswere used to reconstruct the third ray, i.e., if the Au.afarensis hand itself was randomized. Finally, althoughthe multivariate discriminant approach used by Albaet al. (2003) is potentially powerful, it relies on knowl-edge of the length of all medial rays. A single medialdigit, regardless of whether its elements are assignedwith certainty, is sufficient to obtain length ratios ofthumb to medial digit elements in Au. afarensis, as inMarzke (1983). These ratios can then be compared tothe same ratios drawn from extant comparative sampleswhere the sampling procedure mimics the uncertainty inray attribution in the fossil sample. Ratios based on areduced set of elements increase the number of potentialchimeric hands that can be used to obtain a range ofpossible digital proportions in extant hominoids and Au.afarensis, and reduce the impact of misassigning phalan-geal identity in a composite hand on analysis results.

Study design and hypothesis

Because of taphonomic uncertainties associated withhand remains from the Afar, previous assertions thatAu. afarensis had human-like manual proportions seempremature. The inability to assign isolated phalangealelements securely to individual, side or ray at A.L. 333indicates that a more conservative randomizationapproach is necessary, in order to gauge manual propor-tions in extinct hominins when critical information ismissing. Here, we use a randomization method thataccounts for both the inability to determine with anycertainty the number of individuals that contributed tothe sample of complete hand bones at Hadar, and theinability to securely identify isolated phalangeal ele-ments by individual, side, or ray.

Our randomization approach differs from Alba et al.(2003) in that it first generates comparative extant hom-inoid hand samples that match the size and compositionof the Australopithecus hand sample, based on scenariosin which the number of individuals represented in thesample varies (see also Green et al., 2007; Green andGordon, 2008). For each scenario, we then compute threeseparate morphological indices of intrinsic hand propor-tions based on all possible combinations of hand

Fig. 1. Extrinsic phalangeal proportions in Homo, Pan, and Au. afarensis, based on specimen A.L. 288-1 (“Lucy”). The onlymanual proximal phalanx for this specimen has not been securely attributed to side or digit. If it is assumed to come from the thirddigit (Latimer, 1991), then phalanx-to-humerus and phalanx-to-femur length proportions are derived towards the human condition.If the phalanx is from any other digit, however, the ratios are intermediate, and in some cases closer to Pan proportions.

MANUAL PROPORTIONS IN AUSTRALOPITHECUS AFARENSIS 3


elements using both the fossil and extant samples. Ouraims are 1) to generate the largest possible (i.e., mostconservative) ranges of metacarpal, phalangeal and digi-tal ray proportions for Au. afarensis and for extant hom-inoids, and 2) to determine the extent of overlap withinliving taxa, and between extinct and living taxa. We testthe hypothesis that intrinsic manual proportions in Au.afarensis are derived toward the modern human condition.In other words, we predict that manual proportions amongliving forms will be mostly nonoverlapping, and furtherthat the range of resampled intrinsic manual proportionsin Au. afarensis will overlap with the range of Homo only.

MATERIALS AND METHODS

Samples

Fossil sample. All hand specimens attributed to Au.afarensis, and complete enough so that the length of themanual element can be measured accurately, areincluded in the fossil sample. The sample includes meta-carpal and phalangeal elements from the A.L. 333 local-ity (Bush et al., 1982; Ward et al., 2012), metacarpalelements from Hadar locality A.L. 438-1d, as well asphalanges recovered at nearby localities A.L. 288-1, A.L.444 and A.L. 1044. All elements are from the Hadar For-mation, dated between �3.4 and 3.0 MY (Delezene andLucas, 2009), and together the localities cover an area of�4.4 km2 (Hadar Geoinformatics Project: http://iho.a-su.edu/hgp). Many of these elements, including all non-pollical phalanges, cannot be securely ascribed to side,digit identity, or sex. The final sample used to derive themanual proportion metrics in Au. afarensis (see below)comprises a total of 20 bones: one first metacarpal (A.L.333-w39), two third metacarpals (A.L. 333-16 and A.L.438-1d), one proximal thumb phalanx (A.L. 333-69), nineproximal medial phalanges (A.L. 333-w4, -x19, -57, -62,-63, -93, A.L. 288-1x, A.L. 444-4, and A.L. 1044-1) andseven intermediate phalanges (A.L. 333-x18, -32, -46,-64, -88, -149, and -150). Note that we chose thirdmetacarpals as representative of medial metacarpal lengthin our analyses, even though there are other completemedial metacarpals in the Hadar sample (see Ward et al.,2012). Ratios based on the third metacarpal are directlycomparable to the results of Marzke (1983), and have beenshown to correlate well with locomotor function in prima-tes, even when based on composite phalangeal elements(Venkataraman et al., 2013). Further, the two third meta-carpals from Hadar exhibit greater size variation than thetwo complete fifth metacarpals (A.L. 333-14 and -89, Bushet al., 1982), producing a greater possible range of manualproportions for comparison with the resampled extant hom-inoid proportions.

One of the recently recovered elements, A.L. 333-151,was identified as a right intermediate manual phalanx

(Ward et al., 2012). The illustration and description ofthis specimen indicate, however, the strong possibilitythat this element is a proximal phalanx from the firstray. Given the peculiar taphonomy of A.L. 333, wherevirtually no non-hominin faunal remains have beenrecovered (Johanson and Edey, 1982: p 214), it isassumed that this specimen is hominin. Its diminutivesize, however, together with the morphology of the proxi-mal articular facet and trochlea (pers. obs.), suggest thatthis element may be from the first ray of a cercopithe-coid (possibly a papionin foot), which are also present atother localities in the Hadar Formation (Frost and Del-son, 2002). Because of the uncertainty regarding thisspecimen, we did not include it in our analyses.

Extant sample composition. The composition andprovenance of our extant hominoid sample is shown inTable 1, and for the non-human primates comprisemostly wild-shot specimens. All samples are adults ofknown sex with no pathology in the appendicular skele-ton. Specimens were considered adult when their longbone epiphyses were fused or in the process of fusing,i.e., when a gap formerly occupied by the cartilaginousgrowth plate was visible but the epiphyses wereattached to the shaft by bony struts. No corrections forbody mass, sexual dimorphism, or population structurewere applied, as these potentially confounding factorscannot reliably be ascertained in the fossil sample.

Data. Morphological data were derived from the man-ual skeleton from a single side in each individual. Inmost specimens at least one side was available in disar-ticulated form in each limb. In some individuals where acritical element was missing, broken, or showed evidenceof healed fractures, the element was replaced with itshomolog from the contralateral side. Metacarpals fromdigits I and III, as well as proximal and intermediatephalanges of all digits in the hand were placed ventrallyin anatomical position on a flatbed scanner (Microteki320 ScanMaker, Carson, CA) and scanned in TIFF formatat 300 pixels per inch (ppi) (for details on this method, seeYoung and Hallgrimsson, 2005; Rolian, 2009). Distal pha-langes were not included as they are rarely preserved inskeletal preparations. In the extant sample, the identity ofthe phalanges was determined by size and morphologicaldifferences (Susman, 1979; Christensen, 2009), and whenavailable by comparison with the articulated side of theskeleton. No attempt was made to identify the phalangesby side or digit in the fossil sample.

Two-dimensional digital landmarks were placed onhomologous morphological features in each taxon usingTPSDig2 (Rohlf, 2005). Landmarks were used to derive

TABLE 1. Sample composition

Species Males Females Total % Wild Provenance

Homo sapiens 105 108 213 – CMNH, NMNHPan troglodytes 32 56 88 �95 PCM, AMNH, NMNH, MCZGorilla gorilla 53 39 92 �95 PCM, AMNH, NMNH, MCZPongo pygmaeus 17 26 43 �75 NMNH, BSM, MCZTotal 207 229 436

Abbreviations: AMNH, American Museum of Natural History, New York; BSM, Bayerische Staatssammlung, Munich; CMNH,Cleveland Museum of Natural History; MCZ, Harvard Museum of Comparative Zoology, Cambridge, NMNH, National Museum ofNatural History, Washington; PCM, Powell-Cotton Museum, Birchington.



http://iho.asu.edu/hgp

http://iho.asu.edu/hgp

interarticular lengths of metacarpals I and III, and pha-langeal elements from all five digits, using the scalingfactor determined by the scanning resolution (Fig. 2B).For the fossil sample, measurements from the originalHadar collection (Bush et al., 1982) were obtained usingthe same method, from scans of high quality casts in thePeabody Museum at Harvard University. Length meas-urements for the more recent samples in Drapeau et al.(2005) and Ward et al. (2012) (A.L. 438-1d, A.L.444-4,A.L. 1044-1, and A.L.333-149 and -150) were obtained asfollows. Two sets of landmarks were placed on the pub-lished figures showing ventral views of these elements.The first set was placed at morphological features usedto obtain maximum lengths of each element, while thesecond set was placed as in our own measurements (Fig.2B). The ratio of the second to first lengths obtained inthis manner was then used to convert the publishedmaximum lengths to lengths homologous to our own.This ratio method bypasses possible inaccuracies in thescaling of the published photographs. All fossil lengthdata used in the analyses are provided in SupportingInformation Table 1. To account for the possibility thatthe fossil assemblage may contain left-right antimeresfrom the same individual, the length data in extant sam-ples were duplicated. In total, each individual from theextant sample comprises four metacarpal lengths (forMCs 1 and 3 only), 10 proximal phalangeal lengths, and8 intermediate phalangeal lengths.

Analysis. The resampling strategy involves four steps(Fig. 2): 1) obtain random subsamples of extant homi-noids that match the assumed number of individuals (N)in the fossil sample; 2) from these subsamples, randomly

draw a further subsample matching the sample size andcomposition of the fossil hand sample; 3) obtain metricsof manual proportions from the fossil sample and theextant subsamples; 4) repeat steps (2) and (3), i.e.,resample the extant subsamples to derive distributionsof manual proportions and their confidence intervals inAu. afarensis and extant hominoids. Steps (1) to (4) wererepeated for three scenarios in which the fossil assem-blage is derived from a different number of individuals(see below). Procedures in each step are explained inmore detail below. All analyses were run using custom-written routines in R version 3.0.0 (R Core Team, 2013).

Step 1: Drawing subsamples of N individuals. Themanual fossil assemblage at A.L. 333 was not foundarticulated in situ, but scattered over an area of a fewsquare meters (Bush et al., 1982). Given additionalincomplete manual elements and other skeletal remainsat A.L. 333, it is widely accepted that this assemblagecontains more than one individual, perhaps as many asfive (three large- and two-smaller bodied individuals(McHenry, 1992), and possibly as many as nine (Johan-son et al., 1982). Given the composition of the sample ofintact bones at A.L. 333 (Bush et al., 1982; Ward et al.,2012), which includes three complete fifth metacarpals,there is a minimum of two individuals represented inthe fossil sample. The inclusion of A.L. 288-1, A.L. 438-1d, A.L. 444, and A.L. 1044-1 guarantees that the sam-ple comprises at least 6 individuals, and as many as 13.We ran our resampling routines for three scenariosregarding the number of individuals (N): two, five, andten. We include the scenario of N 5 2, even though it ishighly unlikely, to illustrate the effect of deriving

Fig. 2. Summary of resampling protocol. In Step 1 (A, top left panel), a subsample of N 5 2 is randomly chosen from the totalsample of each extant taxon (Table 1), to match hypothetical numbers of individuals represented by the Hadar assemblage. In Step2 (B, top right panel), a sample of manual elements that matches (by type) the sample of complete elements at Hadar is selectedrandomly, without replacement, from the subsamples of individuals derived in Step 1. The black dots in B indicate the location ofthe digital landmarks used to derived lengths of each type of element used in the analysis. In Step 3 (C, bottom right panel), allpossible metacarpal, phalangeal and digital ratios are obtained from the element sample in Step 2, and the minimum, maximumand GM-based ratios are recorded (see text). Step 3 is repeated 10,000 times per taxon, and extant ratio distributions with upperand lower 95% confidence limits are obtained in Step 4 (D, bottom left panel). Steps 1–4 are then repeated for N 5 5 and 10.



manual proportions when the subsamples are assumedto come from very few individuals.

Step 2: Matching the fossil assemblage. Once thesubsample of N individuals was drawn at each iteration,it was further reduced to match the size and compositionof the sample of 20 intact elements in Au. afarensisdescribed above. Identifiable manual elements such asmetacarpals and the first proximal phalanges weredrawn randomly, without replacement, from the knownsample of such elements. In contrast, elements whichcannot be conclusively identified with respect to sideand/or digit identity were first pooled by type (e.g., prox-imal phalanges), and then drawn randomly, withoutreplacement. For example, if the subsample containedthe medial proximal phalangeal lengths of N 5 5 individ-uals (8 phalanges 3 5 individuals 5 40 measurements),then the nine medial proximal phalangeal lengths repre-senting the fossil assemblage were drawn from amongthese measurements.

Step 3: Deriving metrics of manual propor-tions. The hominoid subsamples and fossil sample of21 elements were used to derive metrics describing man-ual proportions in these taxa. We used length ratios toassess manual proportions. Length ratios are univariatereductions of multivariate data, and although they havetheir own methodological shortcomings (e.g., they maynot be scale-invariant, Green and Gordon, 2008), theyare preferable to using residual-based methods that takeinto account some measure of size variation (e.g., Albaet al., 2003). First, unlike ratios, residuals are prone toallometric effects in the sense that the regression linesused to calculate residuals may include size-relatedshape change such that equal residuals may not equatewith equal shape at different sizes (Corruccini, 1978;Jungers et al., 1995). Second, residuals are not actuallya property of individuals, but rather of their relationshipto all other individuals in a sample (Jungers et al.,1995). Third, this method requires choosing a covariateagainst which to measure individual deviations fromexpectation (i.e., the residual), such as body size. How-ever, body size cannot be reliably ascertained for skeletalcollections, let alone fossil samples.

We used three ratios to assess manual proportions: 1)the ratio of the first to third metacarpal (MC) lengths(hereafter the “metacarpal ratio”), 2) the ratio of first tomedial proximal phalanx (PP) length (hereafter the“phalangeal ratio”), and 3) the ratio of first ray to medialray length (hereafter the “digital ratio”), composed of thesummed lengths of the first metacarpal and proximalphalanx, and third metacarpal, medial proximal andintermediate (IP) phalanges, respectively. For each met-ric we took the natural logarithm of the ratio, in orderto normalize data derived from the ratio of two positivenumbers (see Smith, 1999; Green et al., 2007).

Because the fossil sample contains duplicates of someelements, multiple values can be obtained for each ofthese ratios. For the metacarpal ratio, there are 2 suchratios, for the phalangeal ratio, there are 9 possibleratios, and for the digital ratio there are 126 possibleratios, using all combinations of the single first metacar-pal and proximal phalanx, two third metacarpals, nineproximal phalanges and seven intermediate phalanges.To include all possible combinations of manual elements,

and to take into account the possibility that someresampled sets will, by chance, be skewed towardssmaller or larger elements, we report three values foreach of the manual proportions: the minimum ratiowhen using one element of each type (i.e., MC1, MC3,PP1, medial PPs, and IPs), the maximum ratio, and theratio based on the geometric means (GM) of the lengthsof all elements of a given type (e.g., where the geometricmean of the nine proximal phalangeal lengths is used asthe single proximal phalangeal length for calculating thephalangeal and digital ratios).

Step 4: Deriving resampled population distribu-tions. Once Steps 2 and 3 have been completed, man-ual proportions are recorded, and the extantmeasurements are returned to their respective samples.Steps 2 and 3 are then repeated 10,000 times as above,and the measurements for each new extant samplerecorded at each iteration. These 10,000 ratios provideresampled population distributions with means and 95%confidence limits (the lower and upper bounds where95% of the resampled values fall between such boundsby excluding the lower and upper 2.5% of ratios; Manly,2007). In a few cases there are fewer than, or onlyslightly more than, 10,000 unique ways to recombineelements for any given taxon (i.e., MC ratios for Pongo,Pan, and Gorilla when elements are assumed to comefrom two individuals). In these cases, all possible combi-nations of elements are generated exactly once for theextant taxon, and 95% confidence intervals are based onthe exclusion of the upper and lower 2.5% of ratios (i.e.,exact resampling). The distributions are then used toassess the morphological similarity of the Au. afarensismanual proportions to each extant hominoid. Manualproportions in Au. afarensis are considered to be signifi-cantly different from a given hominoid species if the fos-sil ratio under consideration falls outside the 95%confidence interval of that hominoid’s distribution.

RESULTS

Resampled distribution profiles and confidence inter-vals within each type of manual proportion are similarfor a given taxon, regardless of whether 2, 5, or 10 indi-viduals are selected to generate the initial hand sample(Table 2, Figs. 3–5). There is minimal difference betweenthe profiles and confidence intervals for N 5 5 or 10. Thesimilarity in distributions and confidence intervals sug-gests that, at least for these relatively simple lengthratios, hand samples based on five individuals drawn atrandom from larger pools are sufficient to obtain repre-sentative distributions for each metric in each extanttaxon. In other words, although selecting 10 individualsto derive the hand sample in theory increases the rangeof sizes present, it does not appreciably increase theprobability of producing more extreme length ratios.Furthermore, the observed similarity when N 5 2, 5, or10 in extant hominoids suggests the same pattern mightbe expected in fossil taxa such as Au. afarensis. Thus,the comparison of ratios between extant and extincthominins is minimally influenced by the number of indi-viduals (above N 5 1) that are actually represented inthe fossil sample. Note that this statement about howthe comparison is affected is not the same as statingthat the ratio represented in the fossil sample is



minimally affected by the number of individuals that areactually represented.

The resampling procedure provides relatively goodseparation among the distributions of extant hominoidsin all three manual proportions. Pan and Pongo arecharacterized by the lowest (most negative) metacarpal,phalangeal and digital proportions, and both are mostdivergent from Homo, whose ratios are the largest (leastnegative). In all three proportions, Gorilla is intermedi-ate between the other three taxa, but overlaps theirranges. Pan and Pongo are most similar to each other inmetacarpal and digital proportions, while Pan andGorilla are most similar to each other in phalangeal pro-portions (Table 2, Figs. 3–5). The use of ratios precludesdetermining whether a low (negative) value is due tolonger medial digit elements (greater denominator) or ashorter thumb (smaller numerator), or a combination ofboth. Conventionally, the low manual proportions ofchimpanzees and orangutans, as observed here, is attrib-uted to these taxa having both short thumbs and elon-gated medial rays, while the higher ratio of humans isthought to be driven by the reverse situation (Napier,1960). Regardless of the polarity in the difference inlength of manual elements among taxa, however, a morenegative value for the manual metrics indicates agreater length disparity between respective thumb andmedial digital elements. Note that the logarithms for thedigital ratios are negative across taxa, indicating thatthe thumb remains absolutely shorter than the medialdigits, even when sampled from different digital raysand individuals (Fig. 5).

In its metacarpal proportions, Au. afarensis overlapswith the lower end of the 95% confidence interval ofHomo and higher end of the confidence interval ofGorilla (Fig. 3, Table 2), but lies well beyond the confi-dence intervals for Pan and Pongo. This pattern is simi-lar to the metacarpal ratio for Au. africanus reported inGreen and Gordon (2007), and is consistent regardless ofwhether one considers minimum, maximum, or GMratios. In phalangeal proportions, however, Au. afarensisoverlaps the confidence intervals for Homo, Gorilla, andPan, depending on which type of ratio one considers(Fig. 4, Table 2). Using the maximum ratio, all extantratios are shifted positively (i.e., effectively increasingthe length of first ray elements relative to medial ele-ments), resulting in the phalangeal ratio of Au. afarensisfalling within the upper end of confidence intervals forPan and Gorilla, and below the 95% confidence intervalfor Homo (or exactly at the lower confidence limit in thecase of N 5 10). With the minimum ratio, extant phalan-geal ratios are shifted negatively, resulting in the Au.afarensis ratio appearing more similar to modernhumans, although still within the 95% confidence inter-val of gorillas (Fig. 4, Table 2).

A noticeable amount of skew is introduced in to thephalangeal ratios using either the maximum or mini-mum ratio, with minimum ratios having longer negativetails and maximum ratios having longer positive tails(Fig. 4). GM ratios are generally less skewed than eitherof the other two types of ratio. Using the GM ratio, Au.afarensis phalangeal ratio is within the confidence inter-val for Homo, above that of Pan. The fossil ratio is

TABLE 2. 95% confidence intervals for resampling distributions of manual ratios when the fossil and extant samples are assumedto be derived from two individuals

Proportion Method N Au. afarensis Homo Gorilla Pan Pongo

Metacarpal Min 2 20.489 (20.574 to 20.262) (20.849 to 20.379) (20.922 to 20.630) (21.045 to 20.589)GM 2 20.440 (20.510 to 20.233) (20.766 to 20.348) (20.884 to 20.600) (20.953 to 20.564)Max 2 20.390 (20.493 to 20.166) (20.740 to 20.268) (20.860 to 20.548) (20.915 to 20.471)

Phalangeal Min 2 20.609 (20.608 to 20.304) (21.057 to 20.603) (21.097 to 20.671) (21.327 to 20.844)GM 2 20.403 (20.410 to 20.128) (20.856 to 20.434) (20.917 to 20.512) (21.162 to 20.743)Max 2 20.277 (20.237 to 0.136) (20.655 to 20.189) (20.712 to 20.270) (21.023 to 20.570)

Digital ray Min 2 20.749 (20.780 to 20.555) (21.127 to 20.772) (21.196 to 20.938) (21.334 to 20.986)GM 2 20.634 (20.650 to 20.444) (20.978 to 20.655) (21.074 to 20.830) (21.204 to 20.900)Max 2 20.545 (20.532 to 20.285) (20.854 to 20.501) (20.957 to 20.692) (21.109 to 20.770)







Min 5 minimum observed ratio, Max 5 maximum observed ratio, GM 5 ratio based on the geometric mean of each type of element.Values in bold indicate overlap between Australopithecus values and extant hominoid range(s).



within the confidence interval for Gorilla for N 5 5 andN 5 10, but outside it for N 5 2 (Table 2). Phalangealratios in Au. afarensis are well beyond the resampledrange of phalangeal ratios in Pongo in all cases.

Finally, observed digital proportions of Au. afarensisalso overlap the confidence intervals of Homo andGorilla, depending on which type of ratio is considered.For example, the Au. afarensis ratio is within the confi-dence interval for Homo in the case of the minimum andGM ratios, but within Gorilla’s confidence interval inthe case of the maximum digital ratio. This patternreflects the positive shift of all extant taxa when usingthe maximum ratio (Fig. 5, Table 2). Furthermore, GMand maximum fossil ratios are within the confidenceintervals for both humans and gorillas at N 5 10, andwithin one extant species’ confidence interval and justoutside that of the other species at smaller sample sizes.Digital ray proportions are well outside the confidenceintervals for Pan and Pongo in all cases.

Overall, across the three manual proportions, ratiosobtained for Au. afarensis are generally in-between

Gorilla and Homo (as shown in Fig. 4), overlappingtheir respective 95% confidence intervals (Table 2). Inother cases, however, particularly with respect todigital proportions, Au. afarensis proportions are ofteninside the lower confidence intervals of Homo, and mar-ginally outside those Gorilla (though still within itsfull range), although this pattern is also occasionallyreversed. Such reversals are due to the fact thatthe ratio for Au. afarensis is quite close to the bounda-ries of confidence intervals for both Gorilla and Homoin these cases, regardless of which side of the boundaryit happens to fall on in a particular case. In addition,it is important to note that the values obtained forAu. afarensis are also sometimes included within thefull distribution ranges of Pan (Figs. 3–5), especially inphalangeal proportions. In other words, even thoughit is a rare occurrence, it is possible to generateidentical manual proportions between Au. afarensisand each of the African apes and modern humans whenidentical sampling constraints are imposed on eachtaxon.

Fig. 3. Histograms of minimum, GM-based and maximum ratio distributions for metacarpal proportions among extant homi-noids. All histograms are plotted to the same scale, and histograms for N 5 2, 5, and 10 are superimposed on top of each other foreach ratio. White histograms correspond to N 5 2, light gray to N 5 5, and dark gray to N 5 10. Shadings are semitransparent, soareas of medium gray in the middle of each set of histograms corresponds to overlap between all three sample sizes. Ratio valuesfor Au. afarensis are indicated by the dashed vertical line. Extant hominoid distributions whose 95% confidence limits exclude theratio in Au. afarensis are indicated with an asterisk.



DISCUSSION

Manual proportions in Au. afarensis

The objective of this study was to test the hypothesisthat manual proportions in Au. afarensis are essentiallymodern human-like, as suggested by previous studies.The results of our resampling analysis suggest that, con-tra Marzke (1983) and Alba et al. (2003) and our predic-tions, manual proportions in Au. afarensis are moreaccurately described as in between those of Gorilla andHomo, and in some cases indistinguishable betweenthese two taxa. Specifically, metacarpal and phalangealproportions in Australopithecus overlapped the lowerend of the range of Homo as well as the upper end of therange in Gorilla. The resulting digital proportions,which are essentially a combination of the metacarpaland phalangeal metrics, fall between Gorilla and Homo,marginally within the extremes of both distributions.Like Alba et al. (2003) and Marzke (1983), however, ouranalysis confirms that manual proportions in Au. afaren-sis are most dissimilar to Pan and Pongo.

As in Alba et al. (2003) and other studies (e.g., Greenand Gordon, 2007), these conclusions are based on a ran-domization approach designed to address taphonomic

and anatomical uncertainties associated with the fossilrecord at Hadar. Our randomization strategy, however,is more conservative than in Alba et al. (2003), for tworeasons. First, we assume that the fossil sample, giventhe taphonomic context at Hadar, must be derived frommore than one individual. This assumption allows us toinclude all relevant known and complete Au. afarensismanual elements, and to compare this fossil sampleagainst randomized extant assemblages that match itexactly in terms of size and composition. Although Albaet al. (2003) explored the possibility that the compara-tive sample was drawn from multiple individuals, theycompared chimeric extant hands against a single com-posite fossil hand, thus necessarily excluding availableelements from the sample used in their multivariateanalysis.

Second, and related, we did not assign a priori a sideor ray identity to any of the medial phalangeal elements,but assumed instead that they were drawn randomly inthe extant and fossil sample. None of the phalangeal ele-ments from the Afar localities was found in anatomicalconnection, and most are surface finds (Bush et al.,1982). As such, none of the phalangeal elements usedhere (except for the proximal thumb phalanx) can beassigned with any certainty to side or digit. Techniques

Fig. 4. Histograms of minimum, GM-based and maximum ratio distributions for phalangeal proportions among extant homi-noids. Shadings and notations follow Figure 3.



exist for assigning side and ray number to manual ele-ments based on size and/or morphological criteria (e.g.,Susman, 1979; Christensen, 2009). These work best,however, when a near complete set of elements from asingle individual is available, rather than an incompleteset from an unknown number of individuals, as is thecase here. Moreover, the chimeric hands used for theextant sample in Alba et al. (2003) were obtained bymixing elements from different individuals, but fromhomologous manual elements (e.g., the fourth proximalphalanx of one individual is matched with the fourthintermediate phalanx of another, rather than to a differ-ent digital ray). In contrast, we generated intrinsic man-ual length ratios using all possible combinations ofidentifiable (MC 1, MC3, and PP1) and unidentifiablemanual elements (medial proximal and intermediatephalanges).

Our resampling approach generates the largest possi-ble ranges of intrinsic manual proportions for a fossiltaxon, without regard to the side and identity of uniden-tifiable manual elements or to the number of individualsrepresented in a sample. We then match these propor-tions to resampled distributions of extant taxa obtainedin exactly the same manner. Results varied slightlydepending on whether we considered minimum, maxi-mum, or GM ratios of the fossil and extant material. Ofthese three methods, the GM approach incorporates the

most amount of information from the fossil sample (andextant samples) into the calculation of ratios, and alsoavoids the problem of high amounts of skew introducedinto resampled distributions using either of the othermethods. This approach provides the most stringent con-ditions for assessing manual proportions in Au. afaren-sis. If observed proportions under these conditions falloutside the range of specific extant taxa, we can be rela-tively confident that the proportions actually differ.Thus, based on the sample of complete manual elementscurrently available for Au. afarensis, we may concludethat this taxon had manual proportions that were signif-icantly different from Pan and Pongo, with relativelylonger thumbs and/or shorter medial digits. However,because resampled Gorilla and Homo manual propor-tions overlap, and Au. afarensis proportions for the mostpart fall within the range of overlap, we cannot ascer-tain conclusively whether Au. afarensis had Gorilla- orHomo-like manual proportions, particularly with regardto metacarpal proportions.

Taphonomic considerations

Our analyses highlight several taphonomic issues withthe Hadar hand sample. We mention three here,although there may be others. Note that we made noeffort to control for these taphonomic biases in our

Fig. 5. Histograms of minimum, GM-based and maximum ratio distributions for digital proportions among extant hominoids.Shadings and notations follow Figure 3.



analyses. They are important, however, because takentogether they may make the Au. afarensis hand appearmore human-like (or ape-like) than it really is.

Incomplete elements from Hadar may be longer/shorter than those recovered. We used only completeadult Au. afarensis manual elements from multipleHadar localities (Bush et al., 1982; Ward et al., 2012).However, other partial adult manual elements fromHadar preserve sufficient morphology at their proximalor distal ends that their lengths can be estimated, bysimple scaling of dimensions with known complete ele-ments. For example, partial first metacarpal A.L. 333-58is more slender in appearance than A.L. 333-w39 (usedin this analysis), a fact also reflected in the dimensionsof its base and midshaft (Bush et al., 1982). Based onscaling of the known dimensions of the base in these twofirst metacarpals, A.L. 333-58 would probably have beenup to 8–10% shorter than A.L. 333-w39 (Bush et al.,1982). Similarly, the preserved proximal ends of partialthird metacarpal A.L. 333-w6 (Bush et al., 1982) suggestthis bone was �10% longer than A.L. 333-16, one of thetwo third metacarpals we used in our analysis. Ourlength estimates for the partial proximal phalanges fromHadar do not yield lengths outside the range recordedfrom complete proximal phalanges. Hence, the inclusionof these proximal phalanges would not likely change theoutcome of the resampling analyses. However, one of thepartial intermediate phalanges, A.L. 333-w53, has awider base than the largest/longest intermediate pha-lanx in our analysis (A.L. 333-46), and was likely longerby about 5–8% (Bush et al., 1982).

The inclusion of these additional elements would pro-duce a shorter thumb and longer medial digit, thus mov-ing Au. afarensis manual proportions further intoGorilla range. Note that Ward et al. (2012) alsodescribed a fragmentary putative pollical phalanx, A.L.438-4. Using the same scaling strategy with the knowndimensions of A.L. 333-69, the preserved proximaldimensions of this specimen yield a length estimatebetween 33 and 35 mm, or nearly 50% longer than A.L.333-69 (Bush et al., 1982). Such a long PP1 would makeAu. afarensis manual proportions more human-like.However, this length estimate is longer than 90% ofHomo PP1 lengths and all but two Gorilla specimensused in this study. We find it unlikely that such a longPP1 would have been associated with Au. afarensis, ataxon that was absolutely smaller than both of theseextant taxa. It is possible that A.L. 438-4 may instead bea medial phalanx from an Au. afarensis hand (pers. obs.,CR).

There is no intermediate phalanx of an appropriatesize for medial proximal phalanx A.L. 333w-4. Relatedto the above taphonomic bias, the longest proximal pha-lanx, A.L. 333w-4, does not have a matching intermedi-ate phalanx of an appropriate length in the recoveredassemblage of elements, complete or partial. Phalangeallength relationships for each extant taxon can be used toestimate the length of an intermediate phalanx thatwould match A.L. 333w-4 (Supporting Information Fig.1). When the Pan and Pongo scaling relationships areused, the predicted lengths of the intermediate phalanxare 14 and 3% longer, respectively, than the longestavailable intermediate phalanx recovered at Hadar (A.L.

333-46, Bush et al., 1982). When the more likely Homoand Gorilla relationships are used, however, predictedlengths are 14 and 20% longer than A.L. 333-46, respec-tively. A �15% longer intermediate phalanx lowers boththe minimum and GM digital ratios in Au. afarensis,potentially moving it further into the range of gorilladigital proportions.

The medial proximal phalanges are skewedtowards shorter elements. The sample of recoveredproximal phalanges, especially at A.L. 333/333w, may beskewed towards smaller elements. The largest proximalphalanx, A.L. 333w-4, is substantially longer than allothers from A.L. 333, being >15% longer than the nextlongest (A.L. 333-63, Bush et al., 1982). The skewness ofthe total sample of nine Au. afarensis medial proximalphalanges is 11.28, indicating a sampling bias towardsshorter elements. This value exceeds 95% of the skew-ness estimates that were obtained during the resamplingprocedure for each of the extant taxa (data not shown).In other words, the positive skew in the fossil sample ismuch greater than expected by chance alone (since theextant sample proximal phalanges were sampled ran-domly). This skew suggests that longer medial proximalphalanges are under-represented at Hadar. Skewnessmay affect the ratios based on the geometric mean of themedial proximal phalanges, resulting in overestimates ofthe phalangeal and digital ray ratios in Au. afarensis. Inthis case it is useful to consider the results of the mini-mum and maximum ratio analyses to determine whetherall three sets of analyses provide consistent results.Unfortunately, the consideration of these two ratios(phalangeal and digital ray) is where we observe thegreatest variability in the results of the GM, minimum,and maximum ratios. Therefore the best we can say atthis point is that the results are consistent with Au.afarensis having phalangeal and digital ray ratios thatoverlap with those of gorillas and modern humans,albeit at the very upper and lower ends of their respec-tive ranges.

Inferring manipulative abilities in Au. afarensis

Manual proportions have frequently been used to inferthe manipulative ability of fossil hominins (Napier, 1960,1962; Marzke, 1983, Susman et al., 1984). The logicbehind this relatively simple metric is that, amongextant hominoids, humans have a high ratio of thumb tomedial digit length, while apes have relatively shorterthumbs and/or longer medial rays (i.e., a lower ratio). Asa consequence, humans can oppose the tips of the thumband medial digits, while other apes cannot, or do sopoorly (Napier, 1960). Forceful tip-to-tip opposition isthought to be a key precision grip for using and makingstone tools (Marzke and Shackley, 1986). This has beenhypothesized to be an important selective pressure thatled to the evolution of derived manual proportions inhominins, and also one of the main reasons why apes donot, or cannot, habitually make and use stone tools. Ofcourse, some apes make and use tools in the wild(reviewed in Whiten et al., 2009); however, ape lithictools are qualitatively different from Oldowan tools (e.g.,mainly two-handed pounding implements), and requirefundamentally different grips to use (Marzke, 1997).

In theory, the apparent correlation between intrinsicmanual proportions, precision grips and lithic technology



in extant hominoids provides a straightforward predic-tion when it comes to the fossil record. Fossil taxa withprimitive, ape-like proportions should not be associatedwith stone tools, while those evincing derived, Homo-likeproportions should show evidence of stone tool technol-ogy. In practice, however, the correlation between handmorphology, grips and stone tools does not hold up wellin the fossil record. This is especially true for australo-piths, in the critical time period between �4.0 and �2.0MYA, up to and including the first documented appear-ance of stone tools in the archaeological record (Semawet al., 1997). For example, the articulated arm of 3.3 MYAustralopithecus specimen StW 573 from Sterkfontein,South Africa, has a thumb with a “proportion and dispo-sition similar to that of modern man” (Clarke, 1999: p479). No tools have been found with this fossil. Similarly,Kivell et al. (2011) recently described manual propor-tions in A. sediba, a 1.9-million-year-old fossil homininfrom South Africa. Manual proportions in this taxon,based on associated material, are fully Homo-like, with along robust thumb and short medial digits. No stonetools have yet been recovered for this taxon, despite thefact it is considerably younger than the oldest Oldowanartifacts.

Finally, as noted above, all previous assessments ofmanual proportions in Au. afarensis have concluded thatit had human-like manual proportions, and thus shouldhave been capable of tip-to-tip opposition—despite thelack of associated stone tools. The presence of cut marksat the 3.4 MYA site of Dikika, however, does suggestthat tool use was at least potentially within the range ofmanipulative behaviors in Au. afarensis (McPherronet al., 2010). If the marks on the bones from Dikika areindeed the result of tool use, then this would suggestthat the correlation between digit length, precision gripsand stone tools in the hominin fossil record is at bestweak, and perhaps that other grips that do not requireHomo-like proportions (e.g., tip-to-side grips, where thethumb tip opposes the lateral side of the index) were suf-ficient for the use and/or manufacture of particular typesof stone tools, such as flakes, in early hominins.

The lack of association between derived manual pro-portions and lithic technology in these taxa has also ledto alternative explanations for the evolution of derivedmanual proportions in our lineage, for example as pleio-tropic “by-products” of selection acting on correlated phe-notypic traits (Alba et al., 2003; Rolian et al., 2010). Ofcourse, the absence of stone tools does not by itself implythat these hominins were not using other, perhaps non-lithic, implements for extractive foraging, such as sticks,clubs, or leaves. It is also possible that factors otherthan intrinsic hand skeletal proportions, such as cogni-tive capacity, played a role in the evolutionary develop-ment of lithic technology. The results of our analyses areambiguous when it comes to the association betweenmanual proportions, grips and the absence of lithic tech-nology in Au. afarensis. Its intrinsic hand proportionsare at the lower end of the human range and upper endof the gorilla range. This suggests that Au. afarensismay have been capable of opposing the medial digit tipsto the thumb tip, although may have done so with theefficacy of a Gorilla using a tip-to-tip precision grip. Rel-atively little is known regarding precision grip ability inGorilla. In a study of leaf gathering in mountain goril-las, Byrne and Byrne (1993) reported that the tip-to-tipprecision grip was used less frequently than the tip-to-side grip, and both were used less commonly than hook

and power grips involving the movement of all digitstowards the palm. Their preference for tip-to-side gripsmay be due to the intrinsic proportions of the thumband medial digits in this species, as it is in chimpanzees(Marzke and Shackley, 1986).

Alternatively, if Au. afarensis was in fact capable oftip-to-tip and other types of precision grips, then thiswould suggest that the lack of stone tools in this taxonis due to other factors. In a previous study of hand bio-mechanics during simulated Oldowan tool manufactureand use, for example, Rolian and colleagues suggestedthat Au. afarensis may have lacked a sufficiently robustthumb to withstand the types of joint stresses incurredduring manipulative activities (Rolian et al., 2011; seealso Marzke, 1997; Green and Gordon, 2008, and Wil-liams et al., 2012). Specifically, we found that the thumbjoints in humans are exposed to high joint stresses dur-ing simulated Oldowan activities such as hardhammerpercussion and flake use. In Au. afarensis, in which thethumb metacarpal is more gracile and chimpanzee-likethan in humans, such activities would have translatedinto increased relative joint stresses, potentially placingthe hand at greater risk of acute and/or chronic injuries.Moreover, Au. afarensis may have lacked the musclepotential required to produce strong precision grips dur-ing Oldowan activities (Rolian et al., 2011; Tocheri et al.,2008).

Inferring locomotor behavior in Au. afarensis. Therehas been a long-standing debate regarding the extent towhich Au. afarensis engaged in arboreal behaviors, orwas a committed terrestrial biped (Stern and Susman,1983; Susman et al., 1984; Lovejoy, 1988; Latimer, 1991;Ward, 2002). Manual proportions have previously beenused for assessing the reliance on these types of locomo-tor behaviors in extinct hominins by comparison withhomologous proportions in extant primates. For exam-ple, this approach led Latimer (1991) to conclude thatAu. afarensis had abandoned arboreal competence, basedon a perceived similarity in manual proximal phalanx tohumerus length proportions between Lucy (A.L. 288-1)and modern humans. As Figure 1 indicates, however,this similarity may be an artifact of the decision toattribute A.L. 288-10s sole manual proximal phalanx to athird ray. Intermediate and even chimpanzee-like extrin-sic manual proportions can be produced when this pha-lanx is assumed to come from any of the other medialdigital rays.

Admittedly, extrinsic manual proportions, such as theone used by Latimer (1991), or intrinsic hand propor-tions based on the ratio of the length of the digits to thepalm, may be better indicators of the types of below-branch arboreal behaviors practiced by hominoids thanthumb-to-medial digit proportions, as these suspensorybehaviors typically involve the medial digits in hook-likegrips (but see McClure et al., 2012). Notwithstanding,the lowest first-to-third ray ratios in our analyses,observed in Pan and Pongo, happen to correspond to thetwo most arboreal extant species in this sample (Cant,1987; Hunt, 1992; Doran, 1993) while the highest ratioscorrespond to fully terrestrial Homo (Figs. 3–5). Eventhe intermediate ratios observed in Gorilla match themore limited extent of arboreal behavior associated withthis large-bodied taxon (Remis, 1999).

Differences in intrinsic digital proportions among liv-ing hominoids thus reflect to some extent the degree of



arboreality in each, providing insights into arborealbehaviors in fossil hominins. If true, then our resultsremain equivocal with respect to the degree of arboreal-ity in Au. afarensis. Digital ratios in this taxon areclearly higher than the most arboreal apes, suggestingthat Au. afarensis did not rely on the same locomotorand positional behaviors observed in Pan and Pongo, orat least not to the same extent or in the same manner.The metacarpal and digital ratios do overlap withGorilla; however, implying that vertical climbing andother arboreal behaviors may have represented a smallbut significant portion of the positional and locomotorrepertoire of Au. afarensis. This conclusion is compatiblewith other lines of evidence based on the hand (e.g., pha-langeal curvature), upper limb and shoulder girdle, allof which suggest Au. afarensis was a competent treeclimber (e.g., Stern and Susman, 1983; Stern, 2000;Green and Alemseged, 2012).

CONCLUSION

We re-examined manual proportions in Au. afarensisbased on the assemblage of manual elements fromHadar, Ethiopia, in order to re-evaluate previous asser-tions that its intrinsic hand proportions were similar tomodern humans (Marzke, 1983; Alba et al., 2003). Bytaking into account the fact that the Hadar assemblageof manual elements comes from multiple individuals,and includes over 20 complete elements of which onlyfour can be positively identified with respect to side anddigit, we show that intrinsic manual proportions in thisfossil hominin overlap the ranges of both Gorilla andHomo, either falling within the 95% confidence intervalsof both taxa, or falling within the 95% confidence inter-val of one extant taxon and outside the confidence inter-val of the other but close to the boundaries of both.Functionally, our analyses suggest that Au. afarensisshould have been able to produce the types of tip-to-tipprecision grips employed in fine manipulation; however,these grips may not have been as efficient as in modernhumans. This limitation, together with other factorssuch as joint size and muscle potential, may relate tothe absence of stone tools associated with this hominin.Our analyses of intrinsic hand proportions further sug-gest that Au. afarensis may have engaged in limitedarboreal behaviors, similar to extant gorillas. Additionalfossil samples, especially associated upper limb elementsin anatomical connection (Alemseged et al., 2006), willhelp to further refine the range of manipulative abilitiesand arboreal behaviors in Australopithecus afarensis.

ACKNOWLEDGMENTS

The authors are indebted to J. Chupasko (Museum ofComparative Zoology), L. Jellema (Cleveland Museum ofNatural History), L. Gordon and D. Hunt (NationalMuseum of Natural History), E. Westwig (AmericanMuseum of Natural History), M. Harman (Powell-CottonMuseum), D. Hills (Natural History Museum, London) andM. Hiermeier (Bavarian Zoological State Collection) for pro-viding access to specimens in their care. They also thankthe associate editor and reviewers for their comments andsuggestions which helped improve the manuscript.

LITERATURE CITED

Alba DM, Moya-Sola S, Kohler M. 2003. Morphological affinitiesof the Australopithecus afarensis hand on the basis of manual

proportions and relative thumb length. J Hum Evol 44:225–254.

Alemseged Z, Spoor F, Kimbel WH, Bobe R, Geraads D, Reed D,Wynn JG. 2006. A juvenile early hominin skeleton fromDikika, Ethiopia. Nature 443:296–301.

Bush ME, Lovejoy CO, Johanson DC, Coppens Y. 1982. Homi-nid carpal, metacarpal, and phalangeal bones recovered fromthe Hadar Formation—1974–1977 Collections. Am J PhysAnthropol 57:651–677.

Byrne RW, Byrne JME. 1993. Complex leaf-gathering skills ofmountain gorillas (Gorilla g. beringei)—variability and stand-ardization. Am J Primatol 31:241–261.

Cant JGH. 1987. Positional behavior of female Bornean orangu-tans (Pongo pygmaeus). Am J Primatol 12:71–90.

Christensen AM. 2009. Techniques for siding manual pha-langes. Forensic Sci Int 193:84–87.

Clarke RJ. 1999. Discovery of complete arm and hand of the3.3-million-year-old Australopithecus skeleton from Sterkfon-tein. S Afr J Sci 95:477–480.

Corruccini RS. 1978. Primate skeletal allometry and hominoidevolution. Evolution 32:752–758.

Doran DM. 1993. Sex differences in adult chimpanzee positionalbehavior: the influence of body size on locomotion and pos-ture. Am J Phys Anthropol 91:99–115.

Drapeau MS, Ward CV, Kimbel WH, Johanson DC, Rak Y.2005. Associated cranial and forelimb remains attributed toAustralopithecus afarensis from Hadar, Ethiopia. J Hum Evol48:593–642.

Frost SR, Delson E. 2002. Fossil Cercopithecidae from theHadar formation and surrounding areas of the Afar Depres-sion, Ethiopia. J Hum Evol 43:687–748.

Green DJ, Alemseged Z. 2012. Australopithecus afarensis scap-ular ontogeny, function, and the role of climbing in humanevolution. Science 338:514–517.

Green DJ, Gordon AD. 2008. Metacarpal proportions in Austral-opithecus africanus. J Hum Evol 55:358–358.

Green DJ, Gordon AD, Richmond BG. 2007. Limb-size propor-tions in Australopithecus afarensis and Australopithecus afri-canus. J Hum Evol 52:187–200.

Hunt KD. 1992. Positional behavior of Pan troglodytes in theMahale mountains and Gombe Stream National Parks, Tan-zania. Am J Phys Anthropol 87:83–105.

Johanson DC, Edey MA. 1982. Lucy, the beginnings of human-kind. New York: Warner Books.

Johanson DC, Lovejoy CO, Kimbel WH, White TD, Ward SC,Bush ME, Latimer BM, Coppens Y. 1982a. Morphology of thePliocene Partial Hominid Skeleton (Al 288-1) from the HadarFormation, Ethiopia. Am J Phys Anthropol 57:403–451.

Johanson DC, Taieb M, Coppens Y. 1982b. Pliocene hominidsfrom the Hadar Formation, Ethiopia (1973–1977): strati-graphic, chronologic, and paleoenvironmental contexts, withnotes on hominid morphology and systematics. Am J PhysAnthropol 57:373–402.

Johanson DC, Taieb M, Coppens Y, Roche H. 1980. New discov-eries of Pliocene hominids and artifacts in Hadar—interna-tional Afar Research Expedition to Ethiopia (4th and 5th fieldseasons, 1975–77). J Hum Evol 9:583–585.

Jungers WL, Falsetti AB, Wall CE. 1995. Shape, relative size,and size adjustments in morphometrics. Yearb Phys Anthro-pol 38:137–161.

Kimbel WH, Delezene LK. 2009. "Lucy" redux: a review ofresearch on Australopithecus afarensis. Yearb Phys Anthropol52:2–48.

Kivell TL, Kibii JM, Churchill SE, Schmid P, Berger LR. 2011.Australopithecus sediba hand demonstrates mosaic evolutionof locomotor and manipulative abilities. Science 333:1411–1417.

Latimer B. 1991. Locomotor adaptations in Australopithecusafarensis: the issue of arboreality. In: Coppens Y, Senut B,editors. Origine(s) de la bip�edie chez les hominid�es. Paris:Editions du Centre National de la Recherche Scientifique.p 169–176.

Lovejoy CO. 1988. Evolution of human walking. Sci Am 259:118–125.



Manly BFJ. 2007. Randomization, bootstrap, and Monte Carlomethods in biology. Boca Raton, FL: Chapman & Hall/CRC.

Marzke M, Shackley M. 1986. Hominid hand use in the plioceneand Pleistocene: evidence from experimental archaeology andcomparative morphology. J Hum Evol 15:439–460.

Marzke MW. 1983. Joint functions and grips of the Australopi-thecus afarensis hand, with special reference to the region ofthe capitate. J Hum Evol 12:197–211.

Marzke MW. 1997. Precision grips, hand morphology, and tools.Am J Phys Anthropol 102:91–110.

McClure NK, Phillips AC, Vogel ER, Tocheri MW. 2012. Unex-pected pollex and hallux use in wild Pongo pygmaeus wurm-bii. Am J Phys Anthropol 147:S54–S208.

McHenry H. 1992. Body size and proportions in early hominids.Am J Phys Anthropol 87:407–431.

McPherron SP, Alemseged Z, Marean CW, Wynn JG, Reed D,Geraads D, Bobe R, Bearat HA. 2010. Evidence for stone-tool-assisted consumption of animal tissues before 3.39 millionyears ago at Dikika, Ethiopia. Nature 466:857–860.

Napier JR. 1960. Studies of the hands of living primates. ProcZool Soc 134:647–657.

Napier JR. 1962. The evolution of the hand. Sci Am 207:56–62.Napier JR, Tuttle R. 1993. Hands. Princeton, NJ: Princeton

University Press.R Core Team. 2013. R: a language and environment for statisti-

cal computing. Vienna, Austria: R Foundation for StatisticalComputing. Available at: http://www.R-project.org/.

Remis MJ. 1999. Tree structure and sex differences in arboreal-ity among western lowland gorillas (Gorilla gorilla gorilla) atBai Hokou, Central African Republic. Primates 40:383–396.

Rohlf FJ. 2005. TPSDig2. State University of New York, StonyBrook, Stony Brook. Available at: http://life.bio.sunysb.edu/morph/.

Rolian C. 2009. Integration and evolvability in primate handsand feet. Evol Biol 36:100–117.

Rolian C, Lieberman DE, Hallgrimsson B. 2010. The coevolu-tion of human hands and feet. Evolution 64:1558–1568.

Rolian C, Lieberman DE, Zermeno JP. 2011. Hand biomechanicsduring simulated stone tool use. J Hum Evol 61:26–41.

Semaw S, Renne P, Harris JWK, Feibel CS, Bernor RL,Fesseha N, Mowbray K. 1997. 2.5-million-year-old stone toolsfrom Gona, Ethiopia. Nature 385:333–336.

Smith RJ. 1999. Statistical issues with the use of ratios andresiduals as measures of sexual size dimorphism in compara-tive studies. Am J Phys Anthropol:254–254.

Stern JT. 2000. Climbing to the top: a personal memoir of Aus-tralopithecus afarensis. Evol Anthropol 9:113–133.

Stern JT Jr, Susman RL. 1983. The locomotor anatomyof Australopithecus afarensis. Am J Phys Anthropol 60:279–317.

Susman RL. 1979. Comparative and functional morphology ofhominoid fingers. Am J Phys Anthropol 50:215–236.

Susman RL, Stern JT Jr., Jungers WL. 1984. Arboreality andbipedality in the Hadar hominids. Folia Primatol: Int J Pri-matol 43:113–156.

Tocheri MW, Orr CM, Jacofsky MC, Marzke MW. 2008. The evo-lutionary history of the hominin hand since the last commonancestor of Pan and Homo. J Anat 212:544–562.

Venkataraman VV, Rolian C, Gordon AD, Patel BA. 2013. Aresampling approach and implications for estimating the pha-langeal index from unassociated hand bones in fossil prima-tes. Am J Phys Anthropol 151:280–289.

Ward C. 2002. Interpreting the posture and locomotion of Aus-tralopithecus afarensis: where do we stand? Yearb PhysAnthropol 45:185–215.

Ward CV, Kimbel WH, Harmon EH, Johanson DC. 2012. Newpostcranial fossils of Australopithecus afarensis from Hadar,Ethiopia (1990–2007). J Hum Evol 63:1–51.

Whiten A, Schick K, Toth N. 2009. The evolution and culturaltransmission of percussive technology: integrating evidencefrom palaeoanthropology and primatology. J Hum Evol 57:420–435.

Williams EM, Gordon AD, Richmond BG. 2012. Hand pressuredistribution during Oldowan stone tool production. J HumEvol 62:520–532.

Young NM, Hallgrimsson B. 2005. Serial homology and the evo-lution of mammalian limb covariation structure. Evolution59:2691–2704.



reassessing manual proportions in australopithecus afarensis

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