DOI: 10.1126/science.1234598, (2013);340 Science et al.Peter Schmid

Australopithecus sedibaMosaic Morphology in the Thorax of

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Mosaic Morphology in the Thoraxof Australopithecus sedibaPeter Schmid,1,2* Steven E. Churchill,3,2 Shahed Nalla,4,2 Eveline Weissen,1

Kristian J. Carlson,2,5 Darryl J. de Ruiter,6,2 Lee R. Berger2

The shape of the thorax of early hominins has been a point of contention for more than 30 years.Owing to the generally fragmentary nature of fossil hominin ribs, few specimens have beenrecovered that have rib remains complete enough to allow accurate reassembly of thoracicshape, thus leaving open the question of when the cylindrical-shaped chest of humans and theirimmediate ancestors evolved. The ribs of Australopithecus sediba exhibit a mediolaterally narrow,ape-like upper thoracic shape, which is unlike the broad upper thorax of Homo that has beenrelated to the locomotor pattern of endurance walking and running. The lower thorax, however,appears less laterally flared than that of apes and more closely approximates the morphologyfound in humans.

Since the early 1980s, the question of theshape of the thorax of early hominins hasbeen debated (1–6). In apes, the morphol-

ogy of the thorax is integral to the function ofthe upper limb in arboreal locomotion and posi-tional behaviors (7, 8), and thus reconstruction ofthoracic shape in early hominins is central to re-solving questions about the degree of arborealityin members of the human lineage before the genusHomo (9). The study of the evolution of humanthoracic form and function has, however, beenimpeded by the incompleteness of the fossil ribrecord. It has been difficult to reconstruct theoverall shape of this anatomical region owingto the large number of fragile bones of which itis composed and the complex interactions of ribsize, curvature, torsion, and declination that com-bine to determine the shape of the rib cage (thuslimiting the utility of rib fragments). The fragil-ity of costal elements has led to a dearth of bothisolated thoracic remains and the more inform-ative remains associated with partial skeletonsof known species. Even the most complete pre-served early hominin rib cages, such as those ofthe two Australopithecus afarensis partial skel-etons A.L. 288 (Lucy) (10) and KSD-VP-1/1(Woranso-Mille) (6) or the Au. africanus partialskeleton Sts 14 (11), preserve only fragmentaryelements. Nonetheless these, along with the fewfragmentary remains associated with other par-tial skeletons, have stimulated debate over thoracic

shape and the evolution of human-like bipedal-ism and respiratory physiology (1–6).

Both apes and humans have rib cages that aretransversely broad and dorsoventrally flattenedrelative to other catarrhine primates (12). The greatapes also have a rib cage that is conically shapedin anterior view, forming a mediolaterally narrowcupola superiorly and progressively flaring lat-erally from superior to inferior, such that at the

level of the 11th and 12th ribs, the mediolateralwidth of the rib cage matches that of the trans-versely broad iliac blades (12, 13). This config-uration has been linked to arboreal locomotion,in that it effectively positions the ribs so as tobest resist large bending moments generated eitherby the forceful contraction of thoracoscapularand thoracohumeral muscles during support andacceleration of body mass with the upper limbsduring climbing and suspension (14) or by grav-ity operating on body mass during suspension(15). Human thoraces are more barrel-shaped:The upper rib cage is mediolaterally broad, suchthat relatively little additional lateral flaring oc-curs moving inferiorly. Furthermore, the lowerribs in the series have greater curvatures thanthe homologous ribs in apes (16), resulting in arib cage overall that is more cylindrical (barrel-shaped), rather than the funnel shape charac-teristic of apes.

If one assumes that the primitive condition forhominins was an ape-like, conical thorax [butsee (4, 5)], the change to the derived, Homo-likecondition should serve as a potential criticalmarker of the transition from a locomotor reper-toire involving both terrestrial bipedalism andarboreal climbing/suspension (1, 3, 15) to one em-phasizing endurance bipedal walking or running(in which wider shoulders increase the effective-ness of arm-swinging as a means of countering

RESEARCHARTICLES

1Anthropological Institute and Museum, University of Zurich,Winterthurerstrasse 190, CH-8057 Zurich, Switzerland. 2Evo-lutionary Studies Institute, University of the Witwatersrand,Private Bag 3, Wits 2050, South Africa. 3Department of Evo-lutionary Anthropology, Box 90383, Duke University, Durham,NC 27708, USA. 4Department of Human Anatomy and Phys-iology, Faculty of Health Sciences, University of Johannesburg,Johannesburg, South Africa. 5Department of Anthropology,Indiana University, Bloomington, IN 47405, USA. 6Departmentof Anthropology, Texas A&M University, College Station, TX77843, USA.

*Corresponding author. E-mail: smidi@aim.uzh.ch

Fig. 1. Rib remains of MH1 and MH2 in cranial view (see tables S1 and S2). Not pictured:UW88-193 (shaft fragment). UW88-192 derives from a different individual (MH2) than UW88-74/165(MH1) and is only illustrated with those fragments to show its relative anatomical position.

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rotational moments in the trunk) (14, 17). Thus,as the probable precursors of the genus Homo,great importance has been attached to the tho-racic remains of the australopiths, about whichtwo interpretations have emerged. One view isthat australopith remains are largely human inform (2, 5, 6), and thus indicative of essentiallyhuman-like bipedalism, reflecting an ability to bothrun and walk long distances (18). An alternativeview is that their thoracic shape was essentially

ape-like, and thus theywere not only still habitualarborealists, but were incapable of human-likerunning and long-distance walking (3).

More recently, the thorax of the proposed stemspecies of all hominins, Ardipithecus ramidus, hasbeen argued to have been largely derived towardthe human condition (5). This argument is pre-dicated on inferences about the locomotor be-havior of this species and the supposition thata conically shaped thorax is convergently de-

rived in the extant large-bodied apes (4). Thiswould imply that the shape of the thorax in stemhominins was broadly like that of humans, sug-gesting a shift to a fundamentally human-shapedthorax with the earliest establishment of ter-restrial bipedalism in our lineage. However, inAr. Ramidus, the remains of the trunk skeletonare limited to a partial first rib, several associatedcrushed ribs, the neural arches of two thoracicvertebrae, and a fragmentary and distorted pelviswithout a sacrum (5). The poor representation ofthe thorax inAr. ramidus highlights the paucity ofthoracic remains that plague early hominin re-search and urges caution in uncritically acceptingconclusions about thoracic form in this species.

Since mid-2008, the Malapa site in SouthAfrica has yielded a large number of homininfossil remains, most of which are associated withtwo partial skeletons, namely a juvenile probablemale (Malapa Hominin 1: MH1) and an adultprobable female (MH2). Both specimens havebeen ascribed to a new species of early hominin,Au. sediba (19). Postcranial remains of both indi-viduals are well preserved, and aspects of theirskeletons have been recently described (20–22).Both individuals preserve a number of thoracicremains that were found in near articulation andthat elucidate the form of the thorax in Au. sediba.The preserved costal elements (Fig. 1: listed intables S1 and S2) range in completeness fromundamaged or largely complete ribs of both in-dividuals to unidentifiable fragments of the shaftsof lower ribs. In both skeletons, the upper tho-racic region is better preserved than its lower parts.MH1 and MH2 preserve complete first ribs, andMH2 retains proximal portions of the second,third, and fifth ribs, along with a nearly com-plete fourth rib (23). MH1 preserves four partialribs from the lower part of the vertebrosternalseries, including the proximal portions of whatlikely represent the right and left 6th and left 7thribs (23), and shaft fragments that likely derivefrom the left 7th, 8th, or 9th rib. The constella-tion of relatively intact and partial ribs providesinformation about the upper and middle portionsof the thorax: The preservation of a shaft frag-ment from a 9th (or possibly 10th) rib in MH2,along with the well-preserved iliac regions ofboth individuals (21), enables us to reconstructat least the general shape of the lower thoracicregion.

The Upper ThoraxThe overall shape of the upper thorax of Au.sediba is clearly more ape-like, being medio-laterally narrow in the region of the first six ribsto form a typical ape-like apex to the cranial por-tion of the thorax. An ape-like, less acute pos-terior bending of the upper ribs (producing ribsthat flare less laterally, and thus a mediolaterallynarrower rib cage) and possibly a less ventrallypositioned vertebral column [i.e., less invagination;see (24)] in Au. sediba is indicated by its low pos-terior angle index (Fig. 2A) (23). This conclusion isalso supported by the shape index of the second

Fig. 2. Rib curvature in Au. sediba and fossil and extant hominoids. H. sapiens (26 ≤ n ≤ 30), Pa.troglodytes (13≤ n≤ 16), Po. pygmaeus/abelii (11≤ n≤ 12),Hy. lar (n= 20), Au. sediba (n= 2). (A) Posteriorangle (PA) index versus rib number. Larger values of this index reflect ribs that aremore curved at the posteriorangle [see (23)]. (B) Total rib curvature (TRC) index versus rib number. Larger values of this index reflect ribswith shafts that are more curved from the tubercle proximally to the sternal end distally (see 23).

Fig. 3. Rib shape indices [taken following (6)] in the second ribs of Au. sediba (UW88-58), Au.afarensis (KSD-VP-1/1), and extant hominids. Box-and-whisker plots show the median, upper andlower quartiles, and ranges of the Homo sapiens, Gorilla gorilla, and Pan troglodytes samples. Redasterisks denote the index values of the exemplars illustrated below the plots, which have all been alignedby their “costal neck axes” (6). Lower left: the Au. sediba, Au. afarensis, and Pan and Homo second ribshave been overlain in costal neck axis alignment. The parity in curvature is apparent between UW88-58(top) and the chimpanzee 2nd rib, and KSD-VP-1/1 with the human 2nd rib.

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rib [the curvature index of (6)], which in MH2 isestimated to be 78. This value is higher than andoutside of the range of observed values in humans,andwithin that of gorillas and chimpanzees (Fig. 3).This value is also 12 index units above that ofthe KSD-VP-1/1n Au. afarensis second rib (6).

Between-group differences in thoracic shapeare also reflected in indices of rib total curvature(Fig. 2B) (23). In large-bodied apes (Pan andPongo), rib curvature reaches its zenith in theupper vertebrosternal ribs, with the costae be-coming progressively straighter moving inferior-ly to the asternal ribs. However, because of areduction in the angle between the transverse pro-cesses of the thoracic vertebrae and the sagittalplane [angle S of (16)] from superior to inferior,these straighter asternal ribs project more lateral-ly, forming a mediolaterally broad lower thorax.The derived thoracic morphology of H. sapienscan be seen to result from substantially greatercurvature of ribs 2 to 4 (shared homoplasticallywith the barrel-chested Hylobates), which producesa mediolaterally broad upper thorax, combinedwith greater curvature of the lower ribs 9 to 11(not shared with Hylobates), which redirects thelower ribs anteriorly and produces a relativelymediolaterally narrow lower rib cage (16) (andthus a cylindrically shaped thorax overall as seenin anterior view). As with the posterior angle in-dex, Au. sediba has a rib total curvature index atthe fourth rib that is below the mean value ofHomo and most similar to those of Pan and Pongo(Fig. 2B and fig. S9).

The ape-like, conical thoracic shape of Au.sediba is also apparent when the trunk skeleton isrearticulated (Fig. 4). To create a three-dimensionalreconstruction, we articulated ribs R1-5 of MH2

and R6-7 of MH1, using MH2’s thoracic verte-brae T3-7 and interpolating the morphology ofthe T1 and T2 from the preserved vertebrae plusthat of the T2 of MH1 (25). The shape of thethoracic inlet was obtained by articulating theright first rib and the manubrium (fig. S2) in MH2,allowing an appropriate gap for the costal car-tilage. This hemithorax was then mirror-imaged toobtain the upper portion of the complete rib cage.The thoracic inlet shape, as seen from above, ap-pears typically hominoid, being broadly kidney-shaped with the vertebral column positionedventrally (invaginated) within the thorax, but lessso than in modern humans.

The Lower ThoraxIn both apes (7, 26) and humans (16), there iscorrespondence between the shapes of the in-ferior rib cage and the false pelvis (formed by theiliac blades). Thus, the derived, human-like verti-cal reorientation and greater curvature of the iliacblades of Au. sediba (21) lead us to suggest thatits lower thoracic shape could not be like that ofan ape. This inference is supported by a fragmentof a 9th rib (or possibly 10th), found in associationwith the MH2 skeleton. This rib is slenderer thanthe more cranial fragments, a condition very dif-ferent from that of the inferior ribs of apes (whichare the largest and longest in the series). In addi-tion, it appears to show distinct torsion along itsbody, which is characteristic of the reduced lastribs of humans (but not apes) (Fig. 5).

Thoracic Morphology, Respiration,and LocomotionThe thoracic shape of Au. sediba thus appears tobe an unusual combination of the primitive con-

dition of an ape-like upper thoracic shape, witha more derived, human-like shape to the lowerthorax. Thoracic shape in Au. sediba thus maycontrast with that of KSD-VP-1/1, which has beenattributed to Au. afarensis (6), but may not con-trast with another specimen of that species,A.L. 288-1 (1, 3). The morphology of the upperthorax and elements of the pectoral girdle (27)suggest that Au. sediba had habitually elevated,“shrugged” shoulders like that of a chimpan-zee. The shape of the thorax and the position-ing of the scapulae are critical in bipedal gait, asthey affect the pendular mechanics of the up-per limbs in their role as counterbalances to trunkrotation (14, 17). In combination with featuresfound in the foot (22) and lower limb (28), thethoracic shape of Au. sediba implies a gait un-like that predicted for any other early homininspecies. If interpretations of a derived, Homo-like thorax in Au. afarensis are correct (2, 6, 10),it calls into question the possibility that Au. sedibaderives from this species, even via an interme-diate taxon such as Au. africanus, as it wouldrequire a large number of reversals in two formsalready practicing a form of terrestrial bipedal-ism. More critically, if the thoracic region of Ar.ramidus is indeed as derived as recently claimed(5), then by implication, Ardipithecus makes apoor ancestor for at least the lineage leading toAu. sediba.

The morphology seen in the rib cage of Au.sediba also contrasts with that of H. erectus,based on the KNM-WT 15000 juvenile skeleton(16, 29). Mediolateral expansion of the upperthorax in H. erectus (and H. sapiens) has beenargued to be the necessary consequence of nar-rowing of the pelvis and lower rib cage relativeto body size (16) in early Homo. Reduced bi-iliacbreadth (relative to body size) in early Homo mayhave been a response to reduction in gut size fol-lowing from improvement in dietary quality (30),or maintenance of body volume–to–surface arearelationships important to thermoregulation in alineage increasing in stature (31), or was per-haps related to altered energetic or biomechanicaldemands (17, 32–34) of long-distance bipedal-ism in the context of expanded ranging behavior(35, 36). Reductions in the size of the lower ribcage may necessitate expansion of the upper tho-rax to maintain a proper lung volume–to–bodymass relationship (37), and if so, the emergenceof cylindrical thoraces in early Homo may havemore to do with relative reduction in pelvic breadth(16) than with upper limb pendular mechanicsrelated to striding bipedalism or long-distance run-ning (14, 17). However, the mosaic morphologyseen in the trunk of Au. sediba, combining a nar-row upper thorax with a relatively narrow pelvis(21) and (presumably) narrow lower thorax, sug-gests a degree of uncoupling of upper and lowertrunk shape in hominin evolution. This arguesagainst a physiological (lung volume) expla-nation for the Homo thoracic bauplan (espe-cially since Au. sediba appears to compensatefor reduced lower rib cage volume through an

Fig. 4. Two-dimensionalreconstruction of the tho-raxofMH2.Colored areasrepresent parts preservedinMH2[scapula representedby a virtual rendering ofthe original specimen; see(27)].Gray-scale–illustratedbones are associated withMH1 or aremirror-imagedelements from MH2. Lightgray areas represent hy-pothesized outlines.

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anteroposterior, rather than mediolateral, ex-pansion of the upper thorax) (23). In Au. Sediba,we see an incipient development of a narrow,Homo-like waist (with a relatively functionallylong and mobile lumbar vertebral column) (25)with repositioned abdominal oblique muscles thatcan better resist trunk rotation during walking andrunning (32). Au. sediba also appears to exhibitincipient widening of the iliocostalis (fig. S3),which would improve the mechanical advantageof the muscle for counteracting lateral trunk flexionduring bipedal walking (38). However, the narrowupper thorax of Au. sediba, combined with a highscapular position (27) and thus probably incompletedecoupling of the head and pectoral girdle, wouldbe expected to constrain arm-swinging duringwalking or running (17, 32). Furthermore, thismorphology in the upper thorax and pectoral gir-dle would have restricted elevation of the upperpart of the rib cage during inspiration, limiting theability ofAu. sediba to engage in heavy breathingduring fast walking or running (32). A commit-ment to a fully terrestrial life-style in H. erectusmay have relaxed the functional constraints op-erating on early hominin shoulder and upper tho-racic morphology, allowing for a reorganizationof the thorax and shoulder more conducive to thekinematic and respiratory demands of full strid-ing bipedalism and endurance running. This re-organization established the basicHomo thoracic

bauplan (16) seen in all later species of Pleis-tocene Homo (39–41).

References and Notes1. P. Schmid, Eine Rekonstruktion des Skelettes von A.L.

288-1 (Hadar) und deren Konsequenzen [A reconstructionof the skeleton of A.L. 288-1 (Hadar) and its consequences].Folia Primatol. (Basel) 40, 283 (1983).doi: 10.1159/000156111; pmid: 6414917

2. J. C. Ohman, The first rib of hominoids. Am. J. Phys.Anthropol. 70, 209 (1986). doi: 10.1002/ajpa.1330700208; pmid: 3090892

3. P. Schmid, The trunk of the australopithecines, inOrigine(s) de la Bipédie chez les Hominidés. Cahier dePaléoanthropologie, Y. Coppens, B. Senut, Eds. (Editionsdu CNRS, Paris, 1991), pp. 225–234.

4. C. O. Lovejoy, G. Suwa, S. W. Simpson, J. H. Matternes,T. D. White, The great divides: Ardipithecus ramidusreveals the postcrania of our last common ancestors withAfrican apes. Science 326, 100 (2009). doi: 10.1126/science.1175833; pmid: 19810199

5. C. O. Lovejoy, G. Suwa, L. Spurlock, B. Asfaw, T. D. White,The pelvis and femur of Ardipithecus ramidus: Theemergence of upright walking. Science 326, 71 (2009).doi: 10.1126/science.1175831

6. Y. Haile-Selassie et al., An early Australopithecusafarensis postcranium from Woranso-Mille, Ethiopia.Proc. Natl. Acad. Sci. U.S.A. 107, 12121 (2010).doi: 10.1073/pnas.1004527107; pmid: 20566837

7. C. V. Ward, Torso morphology and locomotion inProconsul nyanzae. Am. J. Phys. Anthropol. 92, 291(1993). doi: 10.1002/ajpa.1330920306; pmid: 8291620

8. L. K. Chan, Scapular position in primates. Folia Primatol.(Basel) 78, 19 (2007). doi: 10.1159/000095683;pmid: 17170554

9. C. V. Ward, Interpreting the posture and locomotion ofAustralopithecus afarensis: Where do we stand? Am. J.Phys. Anthropol. 119 (suppl. 35), 185 (2002).doi: 10.1002/ajpa.10185; pmid: 12653313

10. D. C. Johanson et al., Morphology of the Pliocene partialhominid skeleton (A.L. 288-1) from the Hadar Formation,Ethiopia. Am. J. Phys. Anthropol. 57, 403 (1982).doi: 10.1002/ajpa.1330570403

11. J. T. Robinson, Early Hominid Posture and Locomotion(Univ. of Chicago Press, Chicago, 1972).

12. A. H. Schultz, Vertebral column and thorax, inPrimatolgia, H. Hofer, A. H. Schultz, D. Starck, Eds.(S. Karger, Basel, 1961), vol. 4, pp. 1–66.

13. M. Kagaya, N. Ogihara, M. Nakatsukasa, Morphologicalstudy of the anthropoid thoracic cage: Scaling of thoracicwidth and an analysis of rib curvature. Primates 49,89 (2008). doi: 10.1007/s10329-007-0064-z;pmid: 17902025

14. H. Preuschoft, Mechanisms for the acquisition of habitualbipedality: Are there biomechanical reasons for theacquisition of upright bipedal posture? J. Anat. 204, 363(2004). doi: 10.1111/j.0021-8782.2004.00303.x;pmid: 15198701

15. K. D. Hunt, Mechanical implications of chimpanzeepositional behavior. Am. J. Phys. Anthropol. 86, 521(1991). doi: 10.1002/ajpa.1330860408; pmid: 1776659

16. L. M. Jellema, B. Latimer, A. Walker, The rib cage,in The Nariokotome Homo erectus Skeleton, A. Walker,R. Leakey, Eds. (Harvard Univ. Press, Cambridge, MA,1993), pp. 294-325.

17. D. M. Bramble, D. E. Lieberman, Endurance running andthe evolution of Homo. Nature 432, 345 (2004).doi: 10.1038/nature03052; pmid: 15549097

18. C. O. Lovejoy, Evolution of human walking. Sci. Am. 118(November 1988).

19. L. R. Berger et al., Australopithecus sediba: A new speciesof Homo-like australopith from South Africa. Science328, 195 (2010). doi: 10.1126/science.1184944;pmid: 20378811

20. T. L. Kivell, J. M. Kibii, S. E. Churchill, P. Schmid,L. R. Berger, Australopithecus sediba hand demonstratesmosaic evolution of locomotor and manipulative abilities.Science 333, 1411 (2011). doi: 10.1126/science.1202625; pmid: 21903806

21. J. M. Kibii et al., A partial pelvis of Australopithecussediba. Science 333, 1407 (2011). doi: 10.1126/science.1202521; pmid: 21903805

22. B. Zipfel et al., The foot and ankle of Australopithecussediba. Science 333, 1417 (2011). doi: 10.1126/science.1202703; pmid: 21903807

23. Methods and background are available as supplementarymaterials on Science Online.

24. C. O. Lovejoy, The natural history of human gait andposture. Part 1. Spine and pelvis. Gait Posture 21, 95(2005). pmid: 15536039

25. S. A. Williams et al., The vertebral column ofAustralopithecus sediba. Science 340, 1232996 (2013).doi: 10.1126/science.1232996

26. W. C. O. Hill, Observations on a giant Sumatran orang.Am. J. Phys. Anthropol. 24, 449 (1939). doi: 10.1002/ajpa.1330240324

27. S. E. Churchill et al., The upper limb of Australopithecussediba. Science 340, 1233477 (2013). doi: 10.1126/science.1233477

28. J. M. DeSilva et al., The lower limb and mechanics ofwalking in Australopithecus sediba. Science 340,1232999 (2013). doi: 10.1126/science.1232999

29. M. Haeusler, R. Schiess, T. Boeni, New vertebral and ribmaterial point to modern bauplan of the NariokotomeHomo erectus skeleton. J. Hum. Evol. 61, 575 (2011).doi: 10.1016/j.jhevol.2011.07.004; pmid: 21868059

30. L. C. Aiello, P. Wheeler, The expensive-tissue hypothesis.Curr. Anthropol. 36, 199 (1995). doi: 10.1086/204350

31. C. Ruff, A. C. Walker, Body size and shape, inThe Nariokotome Skeleton, A. C. Walker, R. E. Leakey,Eds. (Harvard Univ. Press, Cambridge, MA, 1993),pp. 234–265.

32. P. Schmid, Functional interpretation of the Laetolifootprints, in From Biped to Strider: The Emergence ofModern Human Walking, Running, and Resource

Fig. 5. Ninth rib morphology in Au. sediba, Homo, and Pan. Ribs are shown in superior view on theleft, inferior view on the right. UW88-60, the right 9th rib of MH2, is toward the center and is illustratedtwice in each perspective. Torsion to the superior and inferior margins of the rib (dotted lines) is similar tothat seen in the curved and twisted 9th rib of humans (middle in each perspective) and unlike that of achimpanzee (lateral in each perspective).

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Apr

il 18

, 201

3w

ww

.sci

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Dow

nloa

ded

from

Transport., D. J. Meldrum, C. E. Hilton, Eds. (KluwerAcademic/Plenum, New York, 2004), pp. 49–62.

33. P. A. Kramer, A. D. Sylvester, Bipedal form and locomotorfunction: Understanding the effects of size and shape onvelocity and energetics. PaleoAnthropology 2009, 238(2009). doi: 10.4207/PA.2009.ART32

34. C. N. Shaw, J. T. Stock, The influence of bodyproportions on femoral and tibial midshaft shape inhunter-gatherers. Am. J. Phys. Anthropol. 144, 22(2011). doi: 10.1002/ajpa.21363; pmid: 20623683

35. S. Cachel, J. W. K. Harris, The paleobiology of Homoerectus: Implications for understanding the adaptivezone of this species, in Aspects of African Archaeology,G. Pwiti, R. Soper, Eds. (Univ. of Zimbabwe Publications,Harare, 1996), pp. 3–9.

36. H. Pontzer et al., Locomotor anatomy and biomechanicsof the Dmanisi hominins. J. Hum. Evol. 58, 492 (2010).doi: 10.1016/j.jhevol.2010.03.006; pmid: 20447679

37. P. Gehr et al., Design of the mammalian respiratorysystem. V. Scaling morphometric pulmonary diffusingcapacity to body mass: Wild and domestic mammals.Respir. Physiol. 44, 61 (1981). doi: 10.1016/0034-5687(81)90077-3; pmid: 7232887

38. L. J. Shapiro, W. L. Jungers, Back muscle function duringbipedal walking in chimpanzee and gibbon: Implicationsfor the evolution of human locomotion. Am. J. Phys.Anthropol. 77, 201 (1988). doi: 10.1002/ajpa.1330770208; pmid: 3207169

39. A. Gómez-Olivencia et al., The costal skeleton of Homoantecessor: Preliminary results. J. Hum. Evol. 59, 620(2010). doi: 10.1016/j.jhevol.2010.07.023;pmid: 20965547

40. A. Gómez-Olivencia, K. L. Eaves-Johnson, R. G. Franciscus,J. M. Carretero, J. L. Arsuaga, Kebara 2: New insights

regarding the most complete Neandertal thorax. J. Hum.Evol. 57, 75 (2009). doi: 10.1016/j.jhevol.2009.02.009;pmid: 19540563

41. R. G. Franciscus, S. E. Churchill, The costal skeleton ofShanidar 3 and a reappraisal of Neandertal thoracicmorphology. J. Hum. Evol. 42, 303 (2002). doi: 10.1006/jhev.2001.0528; pmid: 11846533

Acknowledgments: We thank the South African HeritageResource agency for permits to work at the Malapa site; theNash family for granting access to the Malapa site andcontinued support of research on their reserve; the SouthAfrican Department of Science and Technology and the AfricanOrigins Platform (AOP), the South African National ResearchFoundation, the Institute for Human Evolution, University ofthe Witwatersrand, the University of the Witwatersrand’s ViceChancellor’s Discretionary Fund, the National GeographicSociety, the Palaeontological Scientific Trust, the AndrewW. Mellon Foundation, the Ford Foundation, the U.S.Diplomatic Mission to South Africa, the French Embassy ofSouth Africa, the A. H. Schultz Foundation, Duke University,Ray A. Rothrock ’77 Fellowship and IRTAG of Texas A&MUniversity, and the Oppenheimer and Ackerman families andSir Richard Branson for funding; the University of theWitwatersrand’s Schools of Geosciences and AnatomicalSciences and the Bernard Price Institute for Palaeontology forsupport and facilities; the Gauteng Government, GautengDepartment of Agriculture, Conservation and Environment andthe Cradle of Humankind Management Authority; and ourrespective universities for ongoing support. We thank theVirtual Image Processing Lab and the Microfocus X-ray CTfacility of the Palaeosciences Centre at Wits, and forfunding these facilities, we thank the University of theWitwatersrand Office of Research and the NRF Strategic

Research Infrastructure Grant and AOP funding programs.For access to comparative specimens, we thank E. Mbua,P. Kiura, V. Iminjili, and the National Museums of Kenya;B. Billings, B. Zipfel, and the School of Anatomical Sciences atthe University of the Witwatersrand; S. Potze and L. C. Kgasiat the Ditsong Museum; and M. Ponce de León andC. Zollikofer at the Anthropological Institute and Museum.For technical and material support, we thank Duke Universityand the University of Zurich 2009 and 2010 Field Schools.Numerous individuals have been involved in the ongoingpreparation and excavation of these fossils, including C. Dube,C. Kemp, M. Kgasi, M. Languza, J. Malaza, G. Mokoma,P. Mukanela, T. Nemvhundi, M. Ngcamphalala, S. Jirah,S. Tshabalala, and C. Yates. Other individuals who havegiven notable support to this project include B. de Klerk,W. Lawrence, C. Steininger, B. Kuhn, L. Pollarolo, B.Zipfel,J. Kretzen, D. Conforti, J. McCaffery, C. Dlamini, H. Visser,R. McCrae-Samuel, B. Nkosi, B. Louw, L. Backwell,F. Thackeray, and M. Peltier. J. Smilg facilitated computedtomography scanning of the specimens. The Au. sedibaspecimens are archived at the Evolutionary Studies Instituteat the University of the Witwatersrand. All data used in thisstudy are available upon request, including access to theoriginal specimens, by bona fide scientists.

Supplementary Materialswww.sciencemag.org/content/340/6129/1234598/suppl/DC1Methods and ResultsTables S1 to S8Figs. S1 to S11References (42–45)

27 December 2012; accepted 12 March 201310.1126/science.1234598

www.sciencemag.org SCIENCE VOL 340 12 APRIL 2013 1234598-5

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