afar 222

Interpreting the Posture and Locomotion ofAustralopithecus afarensis: Where Do We Stand?CAROL V. WARD*

Department of Anthropology, and Department of Pathology and Anatomical Sciences, University of Missouri,Columbia, Missouri 65211

KEY WORDS bipedality; early hominins; interpretation

ABSTRACT Reconstructing the transition to bipedal-ity is key to understanding early hominin evolution. Be-cause it is the best-known early hominin species, Austra-lopithecus afarensis forms a baseline for interpretinglocomotion in all early hominins. While most researchersagree that A. afarensis individuals were habitual bipeds,they disagree over the importance of arboreality for them.There are two main reasons for the disagreement. First,there are divergent perspectives on how to interpret prim-itive characters. Primitive traits may be retained by sta-bilizing selection, pleiotropy, or other ontogenetic mecha-nisms. Alternately, they could be in the process of beingreduced, or they simply could be selectively neutral. Sec-ond, researchers are asking fundamentally different ques-tions about the fossils. Some are interested in reconstruct-ing the history of selection that shaped A. afarensis, whileothers are interested in reconstructing A. afarensis behav-ior. By explicitly outlining whether we are interested inreconstructing selective history or behavior, we can de-velop testable hypotheses to govern our investigations ofthe fossils. To infer the selective history that shaped ataxon, we must first consider character polarity. Derivedtraits that enhance a particular function, are found to beassociated with that function in extant homologs, and thatepigenetically sensitive data indicate were actually beingused for that function, can be interpreted as adaptations.The null hypothesis to explain the retention of primitivetraits is that of selective neutrality, or nonaptation. Dis-proving this requires demonstration of active stabilizingor negative selection (disaptation). Stabilizing selectioncan be inferred when primitive traits compromise a de-rived function clearly of adaptive value. Prolonged stasis,continued use of the trait for a particular function, or nochange in variability in the trait are evidence that cansupport a hypothesis of adaptation for primitive traits, butstill do not falsify the null hypothesis. Disaptation, ornegative selection, should result in a trait being reduced

or lost. To infer the behaviors of a fossil species, we mustfirst determine its adaptations, use this to make hypoth-eses about its behavior, and test these hypotheses usingepigenetically sensitive traits that are modified by anindividual’s activity pattern. When the A. afarensis dataare evaluated using this framework, it is clear that thesehominins had undergone selection for habitual bipedality,but the null hypothesis of nonaptation to explain the re-tention of primitive, ape-like characters cannot be falsifiedat present. The apparent stasis in Australopithecus post-cranial form is currently the strongest evidence for stabi-lizing selection maintaining its primitive features. Evi-dence from features affected by individual behaviorsduring ontogeny shows that A. afarensis individuals werehabitually traveling bipedally, but evidence presented forarboreal behavior so far is not conclusive. By clearly iden-tifying the questions we are asking about early homininfossils, refining our knowledge about character polarities,and elucidating the factors influencing morphology, wewill be able to progress in our understanding of the pos-ture and locomotion of A. afarensis and all early hominins.Am J Phys Anthropol 45:185–215, 2002.© 2002 Wiley-Liss, Inc.

TABLE OF CONTENTS

Introduction ............................................................................................................................................................. 186Current Hypotheses of Australopithecus afarensis Locomotor Behavior ........................................................... 187Reasons for the Debate ........................................................................................................................................... 188Empirical Frameworks ........................................................................................................................................... 189

Hypotheses about adaptation ............................................................................................................................. 189Hypotheses about behavior ................................................................................................................................. 192

Grant sponsor: NSF; Grant number: SBR 9601025; Grant sponsor:University of Missouri Research Council and Research Board.

*Correspondence to: Carol V. Ward, Department of Anthropology,and Department of Pathology and Anatomical Sciences, 107 SwallowHall, University of Missouri, Columbia, MO 65211.E-mail: [email protected]

DOI 10.1002/ajpa.10185Published online in Wiley InterScience (www.interscience.wiley.

com).

YEARBOOK OF PHYSICAL ANTHROPOLOGY 45:185–215 (2002)

© 2002 WILEY-LISS, INC.

Reexamination of the Fossil Evidence Using This Framework .......................................................................... 192Character polarities and vectors of morphological change in early hominins ................................................ 192Do the derived traits of A. afarensis reflect bipedality? ................................................................................... 197Did primitive traits compromise bipedality? ..................................................................................................... 197Continuing morphological refinement or stasis? ............................................................................................... 200Did A. afarensis actually climb trees? ............................................................................................................... 202

The Many Influences on Morphology .................................................................................................................... 203Implications for Testing Hypotheses About Why Hominin Bipedality Evolved ................................................ 205Summary and Conclusions ..................................................................................................................................... 207Acknowledgments .................................................................................................................................................... 208Literature Cited ...................................................................................................................................................... 208

INTRODUCTION

Bipedality is the hallmark of the human lineage.Whether or not our unique locomotor mode evolvedin the original members of our clade, it represents afundamental adaptive shift away from the apes. Bi-pedality has served as a significant preadaptation tothe acquisition of other key human characteristics,such as tool-making, altriciality of infants, and ar-guably even intelligence. Understanding the natureand timing of the transition to terrestrial bipedallocomotion is key to an accurate interpretation ofhow and why humans evolved.

Over the past 78 years, our knowledge of the na-ture of early hominin (which I define as members ofthe human clade more closely related to us than toPan; see Richmond et al., 2001) bipedality has im-proved dramatically. Dart (1925) correctly inferredthat the Taung child had upright posture, and thatbipedality characterized the earliest part of the hu-man lineage. This interpretation was bolstered byfurther early hominin fossil finds, particularly inSouth Africa, over the next few decades (e.g., Broom,1943; Broom and Schepers, 1946; Le Gros Clark,1947, 1955; Straus, 1948; Broom and Robinson,1949, 1950; Dart, 1949a,b, 1958; Kern and Straus,1949; Broom et al., 1950; Mednick, 1955; Chopra,1962; Napier, 1964, 1967; Day and Wood, 1969;Lovejoy and Heiple, 1970), with interpretations cul-minating in Early Hominid Posture and Locomotion(Robinson, 1972). With the discovery of earlier andmore numerous Australopithecus afarensis1 fossilsin the 1970s (Taieb et al., 1974, 1975; Johanson etal., 1982b and references therein) and footprints atLaetoli (Leakey and Hay, 1979), research on Austra-lopithecus locomotion intensified, and more detailedquestions began to be asked about the functionalmorphology of these hominins.

The debate over hominin locomotion became in-tense in the early 1980s, after the publication of theHadar fossil descriptions, and it continues to thisday. Some researchers have presented data support-ing the hypothesis that Australopithecus afarensisindividuals were obligate bipeds for whom arboreal-ity was adaptively insignificant (Lovejoy et al., 1973;Lovejoy, 1975, 1978, 1988; Day and Wickens, 1980;White, 1980; Latimer, 1983, 1991; Ohman, 1986;Latimer et al., 1987; Latimer and Lovejoy, 1989,1990a, b; Crompton et al., 1998; Kramer, 1999).Others contend that A. afarensis was primarily bi-pedal, yet retained significant adaptations to arbo-reality and thus was partly arboreal (Senut, 1980;Stern and Susman, 1981, 1983, 1991; Feldesman,1982; Jungers, 1982, 1991; Jungers and Stern, 1983;Schmid, 1983; Rose, 1984, 1991; Susman et al.,1984; Deloison, 1985, 1991, 1992; Tardieu 1986a, b;Susman and Stern, 1991; Duncan et al., 1994; Stern,2000), perhaps with a compromised form of bipedalprogression stemming from these retained arborealcharacters (Susman et al., 1984; Preuschoft andWitte, 1991; Rak, 1991; Cartmill and Schmitt, 1996;MacLatchy, 1996; Schmitt et al., 1996, 1999; Ruff,1998; Stern, 1999). At least one researcher arguedthat A. afarensis was not bipedal at all, but was apalmigrade-plantigrade quadruped (Sarmiento,1987, 1994, 1998). The debate is polarized and po-larizing, and is to the point that it impedes ourfurther understanding of the posture and locomotionof early hominins. It serves little further purpose asit has been framed thus far.

Recently, even earlier hominins have been discov-ered. Australopithecus anamensis is now known tohave been a committed biped at 4.2 mya, but ispoorly known postcranially (Leakey et al., 1995,1998; Ward et al., 1999a, 2001). Putative homininsSahelanthropus tchadensis (Brunet et al., 2002) ex-isted 6–7 mya, Orrorin tugenensis about 6 mya (Se-nut et al., 2001), and Ardipithecus ramidus from5.8–4.4 mya (White et al., 1994, 1995; Haile-Selassie, 2001). From the limited data published sofar, the nature of these hominins’ locomotor adapta-tions cannot be fully ascertained. Regardless of whatwe learn about Sahelanthropus, Orrorin, and Ar-dipithecus in the coming years, Australopithecus,and in particular A. afarensis, will remain the basisfor our understanding of the origins and early evo-lution of hominin locomotion. It is the model to

1Some researchers have suggested that because the genus Austra-lopithecus as traditionally defined may be paraphyletic or polyphyl-etic, some species should be removed from Australopithecus andplaced in Praeanthropus or Paranthropus (Senut, 1996, 1999; refer-ences in Collard and Wood, 2000). Because this paper does not con-sider the alpha taxonomy of hominins, and there is no general con-sensus about hominin taxonomy, I will simply refer to all homininspecies originally attributed to Australopithecus (except Ardipithecusramidus) as a single genus, and focus my discussions on functionalinterpretation of the fossils.

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which we will compare the new fossils in order toassess the trajectory of early hominin locomotion,and is central to our understanding of early homininevolution. So, resolving the debate over its locomotorbehavior, and its biology, is still a critical concern ofpaleoanthropology.

CURRENT HYPOTHESES OFAUSTRALOPITHECUS AFARENSIS

LOCOMOTOR BEHAVIOR

The first of three hypotheses suggests that A.afarensis individuals were palmigrade-plantigradequadrupeds (Sarmiento, 1987, 1994, 1998). Thisidea is based primarily on a suite of morphologicalsimilarities between the hands and feet of A. afaren-sis and gorillas, in particular lowland gorillas, whichSarmiento (1987, 1994, 1998) argued are adapta-tions to weight transfer through the fore- and hind-limbs during quadrupedal progression. For example,Australopithecus and Gorilla share shorter fingersand toes than typical for other great apes, a similarmorphology of the hamate-triquetral facet, a morepalmarly directed hamulus and pisiform, broad tib-ialis posterior insertion, and large plantar aponeu-rosis (Sarmiento, 1994).

While these similarities might seem to supportthis hypothesis, the overwhelming suite of skeletalmodifications that enhance bipedal posture and lo-comotion seen in Australopithecus, including the si-nusoidal vertebral curvatures (Robinson, 1972;Ward and Latimer, 1991; but see Sarmiento, 1998),short pelvis with laterally-rotated iliac blades (Jo-hanson et al., 1982a; Tague and Lovejoy, 1986; Love-joy et al., 1999), broad sacrum (Robinson, 1972;Leutenegger and Kelly, 1977), and femoral neckstructure and condyle shape (Lovejoy et al., 1973;Johanson et al., 1982a), are not shared with gorillas,and do not support the hypothesis of quadrupedalposture or locomotion in Australopithecus. In partic-ular, the valgus angle of the knee of hominids is anepigenetically labile trait (Tardieu and Trinkaus,1994; Duren and Ward, 1995; Duren, 1999) anddemonstrates that A. afarensis walked upright notquadrupedally. In a recent study of the developmentof a valgus knee in humans in normal and nonam-bulatory myelodysplastic children, Duren (1999)found that a bicondylar angle was the direct result ofa habitual bipedal gait. It does not form in theseaffected individuals who engage only in intermit-tent, or facultative, bipedality. The presence of avalgus knee in Australopithecus demonstrates thatit was a habitual biped, falsifying the hypothesis ofSarmiento (1987, 1994, 1998). Many shared similar-ities of early hominins and gorillas may be primi-tive, and do not necessarily signify equivalent adap-tations to a particular shared locomotor repertoirein these taxa. Alternately, they could be homopla-sies evolved for different purposes in hominins andgorillas. Therefore, this hypothesis will not be dealtwith further here.

The second hypothesis is the first of two that havereceived much broader support by data and by thepaleoanthropological community. This position hasbeen articulated most clearly and extensively byStern, Susman, and Jungers (summarized by Stern,2000), and states that A. afarensis individuals wereprimarily terrestrial bipeds, but they also climbedtrees (e.g., Senut, 1980; Berge and Ponge, 1983;Jungers and Stern, 1983; Schmid, 1983; Stern andSusman, 1983, 1991; Tardieu, 1986a, b, 1999; Berge,1984, 1991, 1994; Rose, 1984; Susman et al., 1984;Berge and Kazmierczak, 1986; Duncan et al., 1994;Hunt, 1994; Schmitt et al, 1996; Stern, 1999, 2000).These researchers based their conclusions on themosaic of morphological features found in the A.afarensis skeleton (see McHenry, 1994; Stern, 2000).They acknowledged the suite of features reflectingupright bipedal progression, but also emphasizednumerous ape-like characters. They argued thatwhen reconstructing the probable positional behav-iors of A. afarensis, as for any fossil taxon, one mustconsider the total morphological pattern evident in askeleton (Le Gros Clark, 1955; Stern and Susman,1991). From this perspective, all features of an or-ganism are valuable and used, and if there are anyprimitive traits retained in the skeleton, they mustbe there for a functional reason. Some researchershave gone one step further, suggesting that A. afa-rensis exhibits a compromise morphology, and thatthese primitive traits would have affected the na-ture of bipedal progression in Australopithecus(Stern and Susman, 1983; Jungers, 1982; Jungersand Stern, 1983; Rose, 1984, 1991; Susman et al.,1984; Schmitt et al, 1996, 1999; Stern, 1999), result-ing in a bent-knee, bent-hip bipedal progression.

The third hypothesis has also received widespreadsupport. The most widely published proponents ofthis idea are Latimer, Lovejoy, and Ohman, and theclearest articulation of their perspective can befound in Latimer (1991). These researchers also in-terpret the numerous derived features of the A. afa-rensis skeleton as clear evidence of selection for ha-bitual terrestrial bipedality. They note that becauseA. afarensis had not only acquired adaptations forbipedality, it had, in the process, reduced its arbo-real efficiency by sacrificing traits such as relativelylong forelimbs, fingers, and toes, and perhaps mostimportantly, a grasping foot (Latimer and Lovejoy,1989; Latimer, 1991). They cite the clear vector ofmorphological change (defined as the magnitudeand direction of morphological character transfor-mation throughout a lineage; Simpson, 1953) thatwas towards anatomy that enhanced terrestrialbipedality and diminished arboreal competence(Latimer, 1991). Thus, the shift away from featuresenhancing arboreal ability must derive from a be-havioral repertoire in which arboreality was not fa-vored by selection (Latimer, 1991). Hence, arboreal-ity must have been relatively unimportant forsurvival and reproduction in A. afarensis and itsimmediate ancestors. They argue that if A. afarensis

INTERPRETING A. AFARENSIS LOCOMOTION 187Ward]

individuals did climb trees, arboreal agility had lit-tle adaptive significance for them. Although at onepoint Lovejoy (1988) went one step further to addthat A. afarensis not only was not adapted to climbtrees, but could not have done so effectively withoutadverse consequences for their fitness, he later re-turned to the argument that that it simply is notpossible to determine the fitness benefits of arbore-ality in A. afarensis (Ohman et al., 1997).

In summary, these latter two hypotheses aboutearly hominin locomotion are in complete accordover the fact that the recent ancestors of A. afarensishad undergone selection for terrestrial bipedal loco-motion. They differ substantially only over the rel-ative importance of arboreality for A. afarensis.

REASONS FOR THE DEBATE

The first step necessary in unraveling the natureof early hominin bipedality is to understand thenature of the disagreements over interpretations ofA. afarensis locomotion. The debate is not due to alack of fossil evidence, because A. afarensis is knownfrom most skeletal elements. There are a few dis-agreements over interpretations of available fossilevidence (summarized in Stern, 2000), but the de-bate has two more significant causes. First, re-searchers have different approaches to interpretinganatomy, and in particular primitive retentions(Latimer, 1991; Coffing, 1999). Second, and equallyimportantly, they are asking fundamentally differ-ent questions of the data.

One reason for the disagreement over Australo-pithecus locomotion is a fundamental philosophicaldifference in the interpretation of primitive charac-ters (Coffing, 1999). Derived signals in morphologyare relatively easy to interpret. The numerous de-rived traits of Australopithecus have been shown bybiomechanical analyses to be accommodations forweight-bearing and movement in upright bipedalposture. These features, like sinusoidal vertebralcurvatures or an adducted hallux, are unambiguous,and are considered adaptations to habitual uprightposture and locomotion. Their unambiguous polar-ity, coupled with their clear affect on function (in thesense of Lauder, 1996: the use or action of pheno-typic features), reveals their biological role (again asin Lauder, 1996: the role of phenotypic features in aspecific environmental or ecological setting) for bi-pedal progression (Weishampel, 1995). These char-acters tell us that the ability to walk uprightconferred significant fitness benefits on those indi-viduals better designed to deal with the mechanicaldemands of terrestrial bipedality.

The ape-like features of Australopithecus, on theother hand, are generally assumed to be primitiveretentions (lists in McHenry, 1994; Stern, 2000), andmany probably are. Interpreting why these primi-tive features are retained in A. afarensis, or anytaxon, is where perspectives diverge. Australopithe-cus had undergone numerous modifications thatserved to enhance terrestrial bipedal function at the

expense of arboreal function, most notably the lossof a divergent hallux, reduction in intermembralindex, and shorter fingers and toes. These changesimply that agile movement in the trees was of lesserreproductive value than was bipedality for the an-cestors of A. afarensis. This is not to say that arbo-reality was not also selectively valuable, but per-haps it was to a lesser degree. Diminished arborealcompetence did not result in a selective disadvan-tage to the immediate ancestors of A. afarensis,however.

In this case, the retention of features ordinarilyassociated with arboreal progression, such as fore-limbs longer relative to hindlimbs, or phalangeslonger and more curved compared with those of hu-mans, is inherently difficult to explain (see Gouldand Lewontin, 1979; Bock, 1980, Baum and Larson,1991; VanValkenburgh, 1994; Lauder, 1995, 1996).Such traits could have been actively retained bystabilizing selection because they continued to en-hance the survival and reproductive success of theirbearers by enabling them to be more agile treeclimbers than they would otherwise be (adaptations;Gould and Vrba, 1982). Alternately, they may sim-ply have been features that did not compromise ar-boreality and were neither selected for nor against(nonaptations; Gould and Vrba, 1982). They mayeven have been in the process of being selectedagainst (disaptations; Gould and Vrba, 1982). Be-cause any of these three mechanisms can occur, andundoubtedly does occur, these hypotheses are im-possible to test without further information.

Latimer, Lovejoy, and Ohman argue that becausewe cannot readily test these hypotheses, we cannotconsider the adaptive value of retained primitivetraits. Stern, Susman, and Jungers, on the otherhand, argue that the stabilizing selection hypothesisis the only logical one to explain the maintenance ofthe numerous primitive features of A. afarensis. Bi-ases towards one hypothesis can color researchers’interpretations of the adaptive role of morphologicalstructures, and thus the biology and behavior ofextinct animals.

The second, and equally important, reason for thedisagreement over Australopithecus locomotion isthat these two sets of researchers are asking differ-ent questions. Latimer, Lovejoy, and Ohman areinterested in attempting to reconstruct the patternof natural selection that produced A. afarensis: whydid A. afarensis evolve? They would argue that itdoes not matter what actual activities individualsengaged in over the course of the day; the strength ofselection on a particular trait that affects a behavioris not proportional to the time the individual en-gages in that behavior. Individuals sit, sleep, andengage in many other activities that do not imposeadaptively significant consequences on those indi-viduals that do not possess morphologies particu-larly suited to those activities. In other words, allactivities do not have the same fitness effects withrespect to the skeleton. They argue that we simply


cannot know, nor is it necessary to know, all of thebehaviors in which the animals engaged. If we areinterested in reconstructing adaptive history, then itis the vectors of morphological change (Simpson,1953) that will reflect vectors of selection acting on alineage, and provide the answers we seek (Latimer,1991). Stabilizing selection is harder to discriminatefrom lack of selection for primitive structures,Latimer (1991) argues, so we must restrict basingour hypotheses about selective pressures thatshaped a lineage to evidence from directional changewithin that lineage.

Stern, Susman, and Jungers are asking a differ-ent question (Stern and Susman, 1983, 1991; Sus-man et al., 1984; Susman and Stern, 1991; summa-rized in Stern, 2000). They are attempting to inferthe actual behavioral repertoires of A. afarensis in-dividuals, and not the history of selection. Theseresearchers note that individuals engage in variedlocomotor activities over the course of days and life-times. Their approach seeks to identify what types ofbehaviors one might see A. afarensis engaged in ifone traveled back in time to observe them: what wastheir locomotor repertoire? Stern (2000) chooses aquote from Duncan et al. (1994, p. 79) that summa-rizes their philosophy: “understanding the overallfunctional pattern (emphasis mine) of the organismrequires an equal consideration of all its anatomicalfeatures, regardless of whether they are apomor-phies, plesiomorphies or homoplasies. This view-point serves to frame the fossils as once fully func-tional living organism.” Stern, Susman, and Jungersargue that this approach is indeed important, be-cause in order to understand our ancestors, we needto be able to reconstruct their behavior.

These two approaches are different, and comple-mentary rather than mutually exclusive. Thus, theapparent debate as it has been framed is not a truedebate. It is important to keep in mind the distinc-tion between reconstructing behaviors from recon-structing evolutionary pressures. Neither approachto understanding Australopithecus is better or worsethan the other. They are intrinsically different, how-ever. They address the data differently, and rely ondifferent characters for different reasons. Theyshould not be contrasted as opposite sides of a singleargument. Both questions are worth pursuing. Weneed to understand the types of animals early homi-nins were, as well as the history of selection thatshaped them. It is time to recognize the differencesin these approaches, note their inherent limitations,and proceed.

EMPIRICAL FRAMEWORKS

To move forward in our understanding of Austra-lopithecus locomotor behavior, we need to focus ourapproach to interpreting the fossils. The first step isto be explicit about what questions we are asking.Do we want to reconstruct the history of naturalselection shaping the hominin lineage(s), or the lo-comotor/behavioral repertoires of fossil taxa? The

next step is to identify specific hypotheses and cri-teria for their potential falsification. To address thequestion of selective history, we first must under-stand the polarity of traits we are considering, andthe vectors of morphological change apparent in theearly hominin skeleton. To answer either question,we need to better understand morphology and itsinfluences. Not all traits provide similar informationabout fossil taxa (e.g., Cartmill, 1994; Churchill,1996; Lieberman, 1997; Lovejoy et al., 1999, 2000).Some will tell us more about genetic change withina species, and therefore the history of selection, andsome will tell us more about an individual’s behaviorover the course of its lifetime.

Hypotheses about adaptation

To infer the selective regime acting on a speciesfrom morphology alone is notoriously difficult, and asubstantial literature is devoted to this issue (e.g.,Gans, 1966; Gould and Lewontin, 1979; Bock, 1980;Wake, 1982; Arnold, 1983; Mayr, 1983; Baum andLarson, 1991; Leroi et al., 1994; Koehl, 1996; papersand references in Thomason, 1995; Rose andLauder, 1996). Without ecological data and dataabout which behaviors affect fitness in which ways,we lack critical information that would enable us toactually test hypotheses about the selective regimesacting on A. afarensis (Baum and Larson, 1991;Koehl, 1996; Larson and Losos, 1996). Instead, wemust rely on phylogeny, biomechanical modeling,and comparative morphology to support or refutehypotheses about selective pressures as best we can.

To construct hypotheses about the selective re-gime that shaped a taxon, one must first identify thecharacter transformations that occurred in that lin-eage (Felsenstein, 1985; Brooks and MacLennan,1991; Harvey and Pagel, 1991; Kay and Covert,1984; Lauder, 1995, 1996; Weishampel, 1995; Wit-mer, 1995; Larson and Losos, 1996; Begun et al.,1997a,b). This depends on having a reliable phylog-eny from which one can reconstruct ancestral char-acter states. In the case of Australopithecus, molec-ular studies have produced robust hypotheses aboutextant hominoid relationships (see Ruvolo, 1997).This may not be enough to reconstruct the characterstates of the last common ancestor of apes and homi-nins, however. The burgeoning fossil record of Mio-cene and Pliocene apes, including hominins, slowlycontinues to add more data with which to developand test phylogenetic hypotheses among living andfossil taxa. Because these fossil taxa do not resembleextant species in all features, they stand to alter thebalance of parsimony for traits, and so could affectour interpretations of the primitive conditions fromwhich Australopithecus or other early homininsevolved. Continual attention to phylogenetic analy-ses of hominoids will be critical to our ability toreconstruct character transformations that pro-duced Australopithecus and other early hominins.

While drift and other random forces may havelasting impacts on species over time (see Nitecki,


1990), the only evolutionary force that can producelong-term directional change is selection, particu-larly when there is a broad suite of features that allenhance the same function, e.g., bipedality in Aus-tralopithecus. Therefore, it is reasonable to inferthat when long-term directional change is observedwithin a lineage, especially in numerous charactersor character complexes, that selection for a behaviorinfluenced by the observed morphology was thecause.

Biomechanical modeling and comparative studiescan help reveal the biological roles of the newlytransformed structures by determining which func-tion or functions they enhance (Baum and Larson,1991; Weishampel, 1995; Lauder, 1995, 1996). Cou-pling phylogenetic data with biomechanical data al-lows paleontologists to form reasonable hypothesesabout the behaviors on which selection acted. If phy-logenetic analysis determines that a structure isapomorphic, and mechanical analysis determinesthe function it enhances, we can hypothesize thatselection for that function produced the structure(Weishampel. 1995). Comparative morphologicaland behavioral studies can be used to support hy-potheses of adaptation when similarly constructedmodern animals are known to share a similar func-tion. In the case of A. afarensis, there are numerousderived modifications of their skeletons that en-hance terrestrial bipedal progression and resemblemodern hominoid bipeds. Thus, we can hypothesizethat these characters were shaped by selection forbipedal locomotor abilities.

Testing hypotheses about the retention of primi-tive traits is more difficult (e.g., Frumhoff andReeve, 1994). When a primitive trait remains un-modified in a taxon from the ancestral form, the nullhypothesis is that it is selectively neutral, termed asecondary nonaptation (Lauder, 1996). To falsify thenull hypothesis, one must be able to show that sta-bilizing selection or negative selection was at work.To demonstrate stabilizing selection for a primitivetrait, one would need to show that the primitivestructure compromised a derived function. In thecase of Australopithecus, this would be whether itsprimitive traits compromised bipedality.

Other lines of evidence might be invoked asweaker support for the hypothesis of stabilizing se-lection. If a trait was retained in its unmodified formfor a substantial period of time (stasis), it is possible,but not certain, that stabilizing selection was in-volved. If one could demonstrate that an animalactually engaged in behaviors for which the primi-tive traits had been adaptations, it might suggestcontinued adaptive value of these traits, but againthis would not be definitive. Even if these latter twocriteria (stasis or behavior) were met, they wouldstill not falsify the null hypothesis of nonaptation.They merely would be suggestive. If a trait wasselectively neutral, variation should increase overtime (e.g., Tague, 1997, 2002a). However, the lack ofincreased variability still might not signal stabiliz-

ing selection. Even if a trait was neutral with re-spect to selection, a trait could be pleiotropically orstructurally linked to other traits that were underselective influence. Its maintenance could reflectlack of selection to change a developmental cascadeinfluencing other structures that are themselves be-ing maintained by stabilizing selection (discussionsin Maynard Smith et al., 1985; Churchill, 1996).

A final hypothesis for the retention of primitivetraits could be that they were actively being selectedagainst, but that selection had not had sufficienttime to reduce or eliminate them. This hypothesis ofdisaptation would require that the trait would di-minish or change over time, and not persist unal-tered.

A similar conundrum to the issue of arboreality inA. afarensis lies in the interpretation of the rudi-mentary forelimbs in Tyrannosaurus rex (Carpenterand Smith, 2001). Here also is a case where primi-tive features, in this case forelimbs, have been re-tained but altered in the light of a strong directionalsignal towards a new behavior, terrestrial bipedal-ity. So, are these tiny forelimbs still present becausethey serve an adaptive function for some alteredtask, or are they retained for no reason? Some of thedebate over their function takes the form of logicalarguments, which are not necessarily empirical (Os-born, 1906; Newman, 1970; Paul, 1988). The mostrecent contribution uses forelimb bone robusticityand inferred muscle size and strength to argue thatthese are not useless, vestigial structures (Carpen-ter and Smith, 2001). Because both of these featuresare influenced by behavior, this evidence suggeststhat the forelimbs were still used for some purpose,which Carpenter and Smith (2001) hypothesize wasmanipulating food items during oral processing.This case is still different from that in A. afarensis,however, because A. afarensis had not lost the abil-ity to use their primitive ape-like traits for theiroriginal function. It is, however, a useful example toexplore how hypotheses about the functional signif-icance of primitive traits, either adaptive and/or be-havioral, can be tested.

Unlike the Tyrannosaurus example, in which thequestion was if the structure was functional at all ormerely vestigial, a more relevant example is thehindlimbs of the primitive whale Ambulocetus(Thewissen et al., 1994). The retention of functionalhindlimbs in this taxon indicates that it could am-bulate terrestrially, although there was a clear di-rectional signal towards an aquatic lifestyle. Theauthors propose that the hindlimbs were propulsivein the water and on the land. The vector of morpho-logical change clearly was towards improving swim-ming ability at the expense of terrestriality. WhenAmbulocetus was terrestrial, it would have been rel-atively awkward in its movements. Knowing that itcould have moved about on land, and even that itmay have done so, it is still difficult to assess theadaptive significance of terrestriality in these earlywhales. Again, here the fossil record reveals the


vector of morphological change, but reconstructingthe pattern of selection that produced this changerelies on scientific inference.

We also need to be careful not to assume immedi-ately that because Australopithecus did not look ex-actly like humans that its behavior was necessarilydifferent. The retention of primitive traits does notalways mean that these traits were maintained fortheir original function. Examples of discrepancies inform-function relationships between extant and fos-sil taxa can and have been demonstrated betweentooth morphology and diet, for which evidence ofgenetically based morphology (tooth form) can becompared to evidence of behavior (microwear andbone isotope analysis). One example of this phenom-enon was found in the teeth of late Miocene/earlyPliocene horses from Florida (MacFadden et al.,1999). All six species examined in this study re-tained inherited high-crowned molars, and based ontooth morphology would have been interpreted as

grazers of abrasive C4 grasses. However, microwearand isotope data suggest that they had a range ofdiets from browsing to grazing on many types of C3and C4 plants. Some species (particularly Dinohip-pus mexicanus and Astrohippus stockii) were almostexclusively browsers. Hypsodonty appears to havebeen retained, perhaps because of some sort of phy-logenetic and/or developmental constraint, althoughbehavior had changed.

Another example comes from the primate litera-ture. Kay and Ungar (1997) showed that althoughMiocene apes had a similar range of molar shearingcrest lengths as do roughly the same taxonomic di-versity of extant species, the molars of all earlyMiocene taxa were all more bunodont than those ofextant apes (Fig. 1). These data seem to suggest thatno Miocene apes were as folivorous as the mostfolivorous extant apes, i.e., gorillas and siamangs.This may be incorrect, as Kay and Ungar (1997)argued using microwear data. Their microwear

Fig. 1. Molar shearing quotients in extant and early Miocene hominoids. Early Miocene apes have lower crests, but microwearanalyses demonstrate that they had a similar range of diets to extant taxa. This illustrates a disjunction between behavior andanatomy in living and fossil forms. Similar effects could be operating in the postcranial skeleton, but may be more difficult to measure.Figure modified from Kay and Ungar(1997).


analyses showed that, in fact, the Miocene taxa wereeating the same range of diets seen in extant apes,and that even species such as Rangwapithecus,which had teeth with gross morphology most likethose of modern frugivores, were eating as manyleaves as do modern folivores. In effect, tooth mor-phology improved over time.

This may well have happened in the evolution ofhominin, and hominoid, postcranial anatomy, and itmay be possible to uncover the extent to which itmay have occurred by comparing traits with greateror less epigenetic variability resulting from individ-ual behaviors. It underscores the difficulty of inter-preting actual behaviors in fossil taxa.

Hypotheses about behavior

On a practical level, precise interpretation of loco-motor repertoires may exceed the limit of resolutionpossible in the fossil record. For example, humans inmany forager groups like the Yanamamo (Chagnon,1997) and Achuar climb trees for fruit and other foodresources (Descola, 1996a,b). This behavior is notreflected in genetically determined skeletal mor-phology, because anatomical variation that im-proves arboreal abilities apparently has not affectedtheir fitness. We would not be able to “see” thearboreality in their skeletons, just as we cannot“see” behaviors such as lying down or sitting, be-cause an individual’s anatomy does not affect hisfitness by allowing him to be more or less effective atthese behaviors (Latimer, 1991). There is no selec-tive disadvantage of having anatomy that is poorlydesigned for such tasks. This makes interpretingactual behaviors in extinct species particularlytricky. It may be possible at some level, but willalways remain unsatisfying at another. If A. afaren-sis climbed trees, we have to be clever enough to findways to read this in their morphology, potentiallyusing ontogenetically labile characters that can beinfluenced by individual behaviors over the course ofa lifetime. Still, it is worth the attempt, so that wecan better understand what our extinct relativeswere like.

The simple presence of primitive features in the A.afarensis skeleton is not enough to identify theadaptive value of tree climbing. For example, a fu-ture paleoanthropologist studying skeletons of to-day’s humans could argue that because we retaineda grasping hand and mobile shoulder joint, featuresthat evolved for an arboreal lifestyle, modern hu-mans are partly arboreal. None of us, however,would argue that these traits were maintained byselection on humans primarily for the ability toclimb trees well. Instead, these traits primarily rep-resent exaptations for manipulative or throwingabilities, although they also are used in climbingrocks or trees.

Behavior of an extinct animal can be examined byconsidering morphological features that are shapedby its activity pattern. One of the best examples ofan environmentally determined trait is dental mi-

crowear, the pits and scratches on teeth caused bydiet. Given a constant pattern of enamel microstruc-ture and fracture behavior, which appears to be thecase for all hominoids, microwear reveals individualactivity, but not adaptive history (Teaford, 1988,1994). In contrast, because tooth shape appears tobe conservative within taxa, it is generally assumedto be tightly genetically controlled, and not influ-enced by an individual’s diet (although fetal envi-ronment and nutrition may be involved in toothformation, diet appears not to be an influence). Vari-ations in molar shearing crest length among taxa,for example, are thus thought to reflect natural se-lection on crest length in response to diet (Kay andHiiemae, 1974; Kay, 1975; Rosenberger and Kinzey,1976; Strait, 1993a, b; Teaford, 2000). Tooth shapeand features such as molar shearing crest lengthreflect a history of selection, whereas microwear re-flects behavior.

Unfortunately, postcranial anatomy has few, ifany, such dichotomies. Examples of epigeneticallyplastic traits are physeal plate angles (Tardieu andTrinkaus, 1994; Duren, 1999) and diaphyseal cross-sectional form (summarized in Martin et al., 1998;Ruff, 2000), and may also include long bone torsion(Martin and Saller, 1959; King et al., 1969; Sar-miento, 1985; Pieper, 1988) and perhaps even pha-langeal curvature (Richmond, 1998) or aspects ofjoint conformation (Frost, 1979, 1994; Hamrick,1999; but see Lieberman and Pearson, 2001). Bycarefully studying the influences of activity on boneform, either directly or via soft tissues, we will bebetter able to use morphological information reliablyto reconstruct behavior. By identifying the develop-mental plasticity of morphology, we are betterarmed to reconstruct the behavioral repertoires offossils, and to avoid misinterpreting characterswhen constructing phylogenies with morphologicaldata.

REEXAMINATION OF THE FOSSIL EVIDENCEUSING THIS FRAMEWORK

Armed with a more explicit identification of thequestions we are asking about Australopithecus, wecan begin to reevaluate the fossil record for earlyhominin locomotion using this empirical framework.For all phases of this process, it is important toelucidate the genetic and ontogenetic influences onmorphology.

Character polarities and vectors ofmorphological change in early hominins

Reconstructing character transformations withinhominoid lineages is notoriously difficult (Larson,1998; Sarmiento, 1998; Begun, 1999; Richmond etal., 2001). Despite studies arguing that postcranialdata are more informative about phylogeny than arecraniodental data (Collard and Wood, 2000), it is notthe case that we can assume hominins evolved froman ancestor that was similar to extant great apes in


every aspect of its postcranial anatomy. Recent at-tention to the amount of apparent homoplasy in thehominin skeleton (e.g., Larson, 1996, 1988; Begun etal., 1997a, b; Rose, 1997; Ward CV, 1997; Lieber-man, 1999; Coffing and McHenry, 2000; Collard andWood, 2000; MacLatchy et al., 2000) highlights ourneed to remain cautious in making polarity deter-minations, especially based on extant hominoid dataalone. Elucidating the genetic and ontogenetic influ-ences on morphology will aid in the understandingof its phylogenetic signals. Until we better under-stand these effects, we can continue to invoke par-simony arguments if we do cautiously, understand-ing their inherent limitations. We can be mosteffective only by including all available data in con-structing the phylogenies upon which we base ourpolarity determinations.

Character selection determines our ability tomake accurate phylogenetic hypotheses. This re-quires careful choices of features, and knowledgeabout the individual variability, phenotypic plastic-ity, and heritability of traits (e.g., Cartmill, 1994;Weishampel, 1995; Lieberman, 1997, 1999), as wellabout genetic and ontogenetic links among them. Asthe determinants of adult form become clearer, andwe can identify behavioral or functional influenceson morphology, we can use these inferences to makehypotheses about the behaviors of A. afarensis andits ancestors, allowing us to reconstruct the historyof selection that led to bipedality (Richmond andStrait, 2000; Richmond et al., 2001 and referencestherein). Functional anatomy is not unrelated tophylogenetic reconstruction, as it both informs char-acter selection and provides a venue in which to testphylogenetic hypotheses (Brooks and MacLennan,1991; Harvey and Pagel, 1991; Weishampel, 1995;Witmer, 1995; Begun et al., 1997a; Ward et al.,1997). Functional and phylogenetic interpretationsare codependent. Thus, our phylogenetic reconstruc-tions are critical to reconstructing the vectors ofchange.

Based on extant hominoid taxa alone, our percep-tion of character transformation would be relativelystraightforward. All four great ape species share asuite of morphologies that enhance their abilities toengage in vertical climbing and below-branch arbo-real activities, given their relatively large bodysizes. These include a strongly grasping hallux andpollex, a restructured torso involving laterally facingshoulder joints, a high intermembral index, long,curved phalanges, strong manual and pedal grasps,short lumbar vertebral columns, and craniocaudallyelongate pelves. Modern great apes differ in compar-atively minor ways. With no further information,it would seem clear that these shared featureswere indisputably homologous, and that homininsevolved from an ancestor that was postcraniallymuch like extant great apes.

However, extant hominoids are relics from an ear-lier and more diverse age. The vast majority of homi-noid taxa that once existed are extinct. Only by includ-

ing them to reconstruct character transformationthrough hominoids can we come close to uncoveringactual patterns of change in hominoid evolution. Byincorporating Miocene ape fossil data into our phylo-genetic schemes, we may alter the balance of parsi-mony about any number of characteristics (e.g. Begun,1994; Begun et al., 1997a; Rose, 1997; Ward CV, 1997).Determining the phylogenetic relations among fossilapes is problematic, of course. Furthermore, we cannever hope to recover the diversity of hominoid speciesthat must have existed. Nonetheless, without consid-ering what we do know and making careful hypothesesabout the relationships we have identified so far, weneglect vital information about the pattern of evolu-tionary history that produced living hominoids. Thisinformation may alter our perceptions of which homi-nin features are, in fact, derived, and which are prim-itive.

A recently published phylogeny of hominoidsbased on 240 characters of craniofacial, dental, andpostcranial skeletons is the most robust phylogenyof these taxa constructed to date (Fig. 2) (Begun etal., 1997a). Using this as a baseline, we can examinethe likely polarities of the ape-like traits of A. afa-rensis. Not all features are known from the euhomi-noid (the clade including living hominoids; see Fig.2) fossil record, such as proportions within andamong pedal digits, or overall foot length. Still, theapproach will allow us to test hypotheses of adapta-tion, stasis, and disaptation for most characters.

One impact of fossil data on interpreting charac-ter transformations leading to hominins has been inthe realization that extant great apes’ postcranialanatomy may not all be homologous. Sivapithecus iswidely considered to be the sister taxon of Pongo(review in Ward S, 1997). Because humeral torsionis presumed to reflect shoulder joint orientation(Evans and Krahl, 1945; Le Gros Clark and Thomas,1951; Martin and Saller, 1959; Napier and Davis,1959; Larson, 1996, 1998; Pilbeam et al., 1990;Churchill, 1996), and therefore reorganization oftorso structure (Benton, 1965, 1976; Ward, 1993;Ward et al., 1993; Churchill, 1996; but see Chan,1997), this character has particular importance (al-though it can be epigenetically modified by behaviorpattern; Martin and Saller, 1959; King et al., 1969;Sarmiento, 1985; Pieper, 1998). The large Sivapithe-cus parvada humerus from Sethi Nagri (GSP 30754)has less torsion than any extant hominoid, insteadmore closely resembling pronograde quadrupeds(Larson, 1996, 1998; Pilbeam et al., 1990; Madar,1994; Ward S, 1997).2 Furthermore, the Sivapithe-cus postcrania also reveal that members of this ge-nus had less well-developed halluces than do extantorangutans or African apes, and shorter, less curved

2Moya-Sola and Kohler (1996) reconstructed the smaller Sivapithe-cus humerus from a cast, and inferred a different functional pattern.If their conclusion is supported by further analyses, this might indi-cate locomotor diversity within the genus.


phalanges (Rose, 1986, 1997; Spoor et al., 1991;Begun, 1993). Their inferred torso structure, whichreflects a ventrally oriented scapular glenoid fossaeand an emphasis on flexion-extension abilities of theproximal forelimb at the expense of abduction-ad-duction movements, and appendicular charactersperhaps indicating less well-developed manual andpedal grasping ability, are more like those of basalhominoids such as Proconsul (summarized in WardS, 1997).

These Sivapithecus postcranial fossils imply thateither Pongo is convergent upon African apes inmany of its more specialized climbing features, orthat the many craniofacial similarities of Pongo andSivapithecus are homoplasies (Pilbeam et al., 1990;Ward S, 1997). Either of these hypotheses is plausi-ble, but they are mutually exclusive. The possibilityof Asian and African great apes sharing postcranialhomoplasies linked with below-branch arboreality isnot unreasonable, given the apparent independentacquisition of some of these morphologies in Moro-topithecus and atelines (Walker and Rose, 1968;Ward CV, 1993, 1997; Sanders and Bodenbender,1994; MacLatchy, 1996; Rose, 1997; MacLatchy et

al., 2000), suggesting a similar adaptive response inclosely related organisms subjected to similar selec-tive pressures (e.g., Jolly, 2001). The likelihood ofindependent acquisition of the Pongo and Sivapithe-cus craniofacial similarities is less certain at thispoint (Ward S, 1997).

Hominins also share features with fossil “basal”hominoids (Begun and Kordos, 1997; Begun et al.,1997a,b) such as Sivapithecus, Proconsul, and/orEquatorius, and with Hylobates, that are not foundamong extant great apes, such as shorter pelveswith longer lumbar vertebral columns, less curvedforelimb bones, longer thumbs, shorter medial raysof the hand and foot, and less humeral torsion (e.g.,Larson, 1996, 1998; Rose, 1997; Ward CV, 1997;MacLatchy et al., 2000). Foot length is not knownfrom the fossil record after Proconsul, whose feetwere not as long as those of extant apes (Walker andTeaford, 1988). Either hominins have reverted to theprimitive condition in these features, or extant apesare homoplastic in these ways. Either scenario in-volves substantial homoplasy, making polarity de-terminations among hominoids difficult.

Fig. 2. Phylogenetic hypothesis of living and fossil hominoid relationships modified from Begun et al. (1997b). Diagram is aconsensus tree based on 240 cranial and postcranial characters, and so is the most comprehensiveanalysis of these materials publishedto date. Euhominoids refer to clade including all living apes, and basal hominoids to earlier Miocene taxa. Kenyapithecus, Equatorius,and Equatorius were still considered one genus when the analysis was performed, but would all remain basal hominoids if consideredseparately.


The likely Asian-African ape homoplasies openthe possibility that chimps and gorillas may also behomoplastic in some features. This hypothesis issupported by some researchers studying kinematicand anatomical correlates of knuckle-walking inchimps and gorillas (Inouye, 1994; Dainton and Ma-cho, 1999). If so, some of these hominin charactersmay be primitive, which would indicate less changefrom the last common ancestor than we now sup-pose. Recently, however, strong arguments weremade in favor of the hypothesis that the last com-mon ancestor was a knuckle-walker, and that Afri-can ape postcranial similarities are indeed homolo-gous (Richmond et al., 2001). This perspective is themost widely accepted at present. Further researchinto the function and evolution of the forelimb isneeded to continue to test these competing hypoth-eses.

Most A. afarensis traits interpreted as primitive,based on comparison with extant taxa (McHenry,1994; Stern, 2000), still appear to be primitive evenwhen the fossil evidence is considered. A long pisi-form, dorsoplantarly narrow navicular, and meta-tarsals lacking expanded dorsal margins of theirhead are known for Oreopithecus (Sarmiento, 1987)and extant apes. Australopithecus lacks the ex-panded vertebral bodies of humans, resembling alltaxa for which there are data (e.g., McHenry, 1992):Proconsul (Napier and Davis, 1959; Walker andPickford, 1983; Walker and Teaford, 1988; Ward etal., 1993), Nacholapithecus (Rose et al., 1996a,b;Nakatsukasa et al., 1998, 2000), Equatorius (LeGros Clark and Leakey, 1951), Morotopithecus(Walker and Rose, 1968; Gebo et al., 1997; Mac-Latchy et al., 2000), Oreopithecus (Harrison, 1986;Sarmiento, 1987), Dryopithecus (Moya-Sola andKohler, 1996), and extant primates. Within thehand, a pronounced third metacarpal styloid pro-cess, found only in Homo and some gorillas, is ab-sent in Proconsul (Napier and Davis, 1959) andOreopithecus (Moya-Sola et al., 1999). Also, the firstmetacarpal base highly is concavoconvex in Procon-sul (personal observation), Sivapithecus (Spoor etal., 1991), Oreopithecus (Moya-Sola et al., 1999), andextant apes. Small apical tufts are found on thedistal phalanges of Afropithecus (Leakey et al.,1988), Proconsul (Napier and Davis, 1959; Begun,1994), Nacholapithecus (Nakatsukasa et al., 1998),Oreopithecus (Moya-Sola et al., 1999), Dryopithecus(Moya-Sola and Kohler, 1996), and extant primates.The mediolaterally broad knee joint, typical of ex-tant apes and seen to a lesser extant in A. afarensis(Tardieu, 1979, 1981), is also known for Proconsul(Walker and Pickford, 1983) and Oreopithecus (Har-rison, 1986; Sarmiento, 1987).

Many primitive traits, however, are derived to-ward a human-like condition from the ape-like one.Long, curved phalanges with pronounced flexorridges are found in Oreopithecus (Harrison, 1986;Sarmiento, 1987; Moya-Sola et al., 1999), Dryopithe-cus (Begun, 1992, 1993; Moya-Sola and Kohler,

1996), Orrorin (Senut et al., 2001), and Ardipithecus(Haile-Selassie, 2001), and in extant apes, althoughless so in early hominoid taxa (Begun, 1994; Rose,1997). Australopithecus appears to have had re-duced manual and pedal phalanges that were rela-tively shorter than in any primate except Homo(Bush et al., 1982; White, 1994).3 The hamate ham-ulus is only somewhat distally directed, intermedi-ate between extant apes and humans (Sarmiento,1994, 1998; Ward et al., 1999b). The large hamulusappears to be found only in African apes and homi-nins, and is not present in Sivapithecus (Spoor et al.,1991) or Proconsul (Beard et al., 1986). Hamulusform likely reflects morphology of the carpal tunnelrather than flexor carpi ulnaris function, as previ-ously suggested (Sarmiento, 1998; Ward et al.,1999b). However, the pisohamate ligament insertsnot on the distal end of the hamulus, but at its base,at least in chimpanzees and humans (personal ob-servation). Thus, hamulus size and orientation ap-pear not to reflect the flexor carpi ulnaris muscle orpisohamate ligament, but the palmar carpal liga-ment (flexor retinaculum), which forms the roof ofthe carpal tunnel. It is certainly possible that carpaltunnel length is related to overall hand length, andif so, hamulus distal projection may be related tohand length at least at some level. A. afarensis ap-pears to have reduced the proximodistal length of itscarpal tunnel relative to African apes.

The high intermembral index (calculated as (hu-merus � radius/femur � tibia) * 100) of African apesappears to have been present in at least Oreopithe-cus (Hurzeler, 1960; Moya-Sola and Kohler, 1996)and Dryopithecus (Moya-Sola and Kohler, 1996), al-though not in Proconsul (Walker and Pickford, 1983;Walker and Teaford, 1988). Although Dryopithecuswas interpreted to have an intermembral indexhigher than that of African apes and only like oran-gutans among extant species (Moya-Sola andKohler, 1996), it may not have been as extreme, asthese data were based on extensive segment lengthreconstructions. Direct comparison of the reportedulna to femur lengths published with the fossil an-nouncement (Moya-Sola and Kohler, 1996) is 102,close to the African ape range (chimpanzees, 87–97;gorillas, 91–101), and considerably less than that oforangutans (128–130). Oreopithecus, on the otherhand, is intermediate between extant African andAsian apes, with an ulna/femur ratio of 111. Austra-lopithecus had an ulna (length estimate based onDrapeau, 2001) to femur length of about 80, showingan apparent reduction in forelimb to hindlimb pro-portions. This is evident in comparisons of humeralto femoral proportions as well (Jungers, 1982, 1994;Wolpoff, 1983; White et al., 1993; White, 1994).

3In this paper, the term Homo is used to include Homo erectus/ergaster and more recent members of the genus Homo only, followingthe grade-based approach of Wood and Collard (1999).


Within the forelimb, A. afarensis also appears tobe primitive in arm, forearm, and metacarpal seg-ment lengths (Drapeau, 2001). By including the A.afarensis partial skeletons AL 288-1 and AL 438-1,along with extant cercopithecids, Dryopithecus, andOreopithecus, she demonstrated that the slightlyhigher brachial index of Australopithecus comparedwith extant apes (see Kimbel et al., 1994) appears torepresent the primitive large-hominoid condition. A.afarensis does not appear to have shortened its up-per limbs from the primitive condition, nor length-ened them, showing less directional change thanoften assumed (Jungers, 1982, 1994; Wolpoff, 1983;White et al., 1993; White, 1994). There is thus noevidence that A. afarensis is derived in forelimbproportions, supporting the hypothesis that theirlower limbs are elongated rather than their fore-limbs reduced (Wolpoff, 1983). Instead, Pan andPongo, and to a lesser extent Gorilla, seem to haveindependently elongated their forearms from thelikely ancestral condition.

Another important finding by Drapeau (2001) isthat chimpanzees and bonobos have uniquely longmetacarpals relative to their forearm lengths amongextant and fossil hominoids. Australopithecus meta-carpals are the same length relative to the forearmsas in all extant hominoids except Pan. This discov-ery highlights the potential error in assuming thatPan reflects the morphology of the last commonancestor.

A number of primitive characters of A. afarensisappear to reflect soft-tissue differences from hu-mans, and suggest a somewhat more extant greatape-like muscular configuration in these early homi-nins. Some of the Australopithecus hip and thighmuscle attachment sites appear to have differedfrom those of Homo. Instead, they more closely re-semble those of extant apes, and as best as can bedetermined, fossil taxa as well. First, there is alarge, roughened ovoid area on the anterolateralborder of the greater trochanter (Fig. 3), which ap-pears to have been for attachment of the anteriorfibers of gluteus minimus, which on great apes issometimes a separate muscle called the scansorius.In humans, this muscle attaches on the anterosupe-rior portion of the trochanter, and does not extenddistally. Hausler (2001) reconstructs the glutealmuscles of A. afarensis and A. africanus as essen-tially human-like, although with a slightly ex-panded anterior portion of the gluteus medius (con-tra Berge, 1994). These observations are consistentwith the hypothesis of Robinson (1972) that thelarge anterior lesser gluteals could compensate bythe slightly less sagittal orientation of the iliacblades.

The medial thigh muscles of A. afarensis also ap-pear to have differed in their distal insertions. Inhumans, the sartorius, gracilis, and semitendinosushave a common fan-shaped insertion called the pesansirinus that largely blends with the crural fasciaalong the medial side of the proximal tibia. In A.

afarensis, however, these muscles had an extantape-like conformation, with a discrete bony insertionalong the medial margin of the tibial tuberosity,leaving a roughened pit in the bone (Fig. 3). Al-though there is no bony evidence of it, on the lateralside of the knee in chimpanzees and gorillas, thebiceps femoris extends to the lateral side of the tibialtuberosity but blends with the crural fascia, with noevident bony insertion (personal observation). It isat least possible that this would have been the casein Australopithecus, given the ape-like medial sideof the knee. The conformation of the A. afarensisischial tuberosity also differs from that of humans,being longer, with the adductor magnus origin siteset at an angle to the rest of the tuberosity. Thisdifferent conformation may reflect other primitivemusculature.

Latimer and Lovejoy (1990b) suggest that the con-vex first metatarsal head of A. afarensis, unlike theflatter configuration in humans, may reflect moreidiosyncratic loading in A. afaernsis than in Homo.They argue this may be due to the fact that thetriceps surae may not yet have undergone thechanges in muscle belly length and pennation seenin humans, and so relatively more plantarflexionwas accomplished with the peroneal muscles. Thelarge peroneal muscles are suggested by the largeperoneal groove on the fibula and peroneal trochleaon the calcaneus (Latimer and Lovejoy, 1989,1990b). This hypothesis is difficult to test, as mus-cles do not fossilize. Given the lack of capacity for

Fig. 3. Proximal femurs and tibias of Homo sapiens, Austra-lopithecus afarensis AL 288-1, and Pan troglodytes. Note similarlocation of presumed muscle attachments in A. afarensis and inchimpanzee. Line drawings modified from Aiello and Dean(1990).


hallucal abduction in any Australopithecus, it ishighly unlikely that the rounded head of the firstmetatarsal reflects opposability, but whether itsomehow reflects arboreality is unspecified and un-known.

Taken together, though, these indicators of asomewhat primitive muscle configuration in Austra-lopithecus suggest that these early hominins werenot fully modern in their muscular anatomy. This isan important point, because when muscles contractto respond to ground reaction forces or producemovement, they generate strain within bones thatcan trigger modeling responses during growth andremodeling after skeletal maturity (review and dis-cussion in Martin et al., 1998; Carter and Beaupre,2001). This means that some bony differences be-tween Australopithecus and humans could be re-lated to one of two factors, or both. Either thesehominins were behaving differently, or they werebehaving in the same way but with slightly differentmuscle vectors due to the primitive muscle arrange-ment. The latter situation could produce a slightlydifferent pattern of bone strain, influencing traitssuch as the geometry of the acetabulum, proximalfemoral shaft, patellar groove, or hallucal tarso-metatarsal joint shape. Indeed, Berge (1991) hy-pothesized that A. afarensis only could have movedbipedally efficiently if it had a more ape-like ar-rangement of the hip musculature due to its slightlydifferent bone structure. Although these ideas havenot been tested, they represent a plausible alternatehypothesis that should be considered when evaluat-ing skeletal differences among hominins.

Another feature in which A. afarensis has beenconsidered significantly different from humans is inthe anteroposteriorly compressed sacral ala. How-ever, given the mediolaterally extensive and antero-posteriorly compressed nature of the A. afarensispelvis, and the broadly flaring blades, this featuremay simply reflect iliac form and may not be a rel-evant variable itself (see Lovejoy et al., 2000).

A final line of evidence we can use to assess char-acter polarities involves the few data now availablefor the earliest putative hominins Sahelanthropus,Orrorin, and Ardipithecus. All three genera havebeen described as probable bipeds, but the nature ofthis bipedality and their morphological similarity tolater hominins are still unknown or undescribed.Sahelanthropus is known only from a cranium. Be-cause it has a short basicranium with the basionintersected by the bicarotid cord, like other homi-nins, its discoverers tentatively suggest it was up-right, barring further evidence (Brunet et al., 2002).A nearly complete femur is known for Orrorin,which its discoverers say displays bipedal features(Senut et al., 2001). None of the characters theymention in their article, however, are exclusivelyfound in bipeds. It could be that when the internalcontours of the femoral neck are revealed, and whenproximal to middle shaft dimensions are compared,the data will be sufficient to make a judgment. Ar-

dipithecus has also been described as a biped, basedon a short basicranium in A. ramidus ramidus(White et al., 1994) as in Sahelanthropus (Brunet etal., 2002), and on a proximal phalanx of A. ramiduskedabba that resembles those at Hadar (Haile-Selassie, 2001). A. r. kedabba also appears to havehad a curved ulna, but this is found in homininulnas from the Omo River Valley (Omo L40-19) andOlduvai Gorge (OH 36). The published forearm re-mains of A. r. ramidus appear more like those of A.afarensis than African apes, but few details havebeen published so far.

So, in summary, most features of A. afarensis thatare generally interpreted to be primitive probablyare, although the prevalence of homoplasy amonghominoids should suggest caution in making thisassumption. The likely homoplasies between Asianand African apes raise the possibility that Africanapes may be convergent upon one another in waysother than forelimb length, making some apparentlyderived hominin features possible homoplasies, suchas relatively short forelimbs, short pelves, 5–6 lum-bar vertebrae, and thumb-finger proportions. Thiscould be true even if the last common ancestor ofAfrican apes and humans was a knuckle-walker.Some features that appeared to be derived in A.afarensis, such as the short metacarpals or forelimbproportions, appear to be primitive, with extant apesoften displaying a derived condition. Extant apescannot be assumed to represent the primitive condi-tion, illustrated by the autapomorphic, relativelylong metacarpals of Pan. Ignoring the Miocene fossilrecord obscures potentially critical information, andnew fossils will certainly help answer the questions.

Do the derived traits of A. afarensisreflect bipedality?

Because there is such an extensive literature onthis subject, I will not review it here. Derived traitlists and discussions of their significance can befound in McHenry (1994) and Stern (2000), and arereviewed in Aiello and Dean (1990). The skull, ver-tebral column, pelvis, and entire lower limb all re-flect clear and unambiguous characters recognizedas adaptations for upright, bipedal progression bynumerous mechanical analyses. They are all traitsshared at least to some extent with humans, theonly bipedal hominoids. These changes and theirsimilarities to modern humans are far more exten-sive than the differences due to retained primitivecharacters. This suggests that they were indeed ad-aptations shaped by natural selection for bipedalposture and locomotion (Weishampel, 1995; Lauder,1996).

Did primitive traits compromise bipedality?

To test whether or not primitive traits were re-tained by stabilizing selection, we first need to con-sider whether they compromised the derived func-tion. In other words, we need to test whether the


retained features presumed to be adaptations forarboreality compromised bipedal locomotion.

Some researchers have implied that the gait of A.afarensis differed from that of humans because theyhad slightly different limb proportions, muscle at-tachment sites, and a pelvis with less coronally ori-ented iliac blades and a smaller anterior horn of theacetabulum than do humans. Some have suggestedthat this indicates the bipedal gait of A. afarensiswas more energetically expensive than that of hu-mans, or at least different (Berge, 1991; Cartmilland Schmitt, 1996; Preuschoft and Witte, 1991; Rak,1991; Rose, 1984, 1991; Ruff, 1998; Schmitt et al.,1996, 1999; Stern, 1999; Susman et al., 1984; Tar-dieu, 1991). Even if it is true that Australopithecusmight have looked different when it walked than doextant humans (Jungers, 1984; Rak, 1991; Schmittet al., 1996; Ruff, 1998; Schmitt et al., 1999), itremains to be demonstrated that they were lesscapable bipeds, or if they differed from us, exactlyhow. If Australopithecus could not walk as fast, far,or well as do humans, and this was because of theretention of traits that enhanced arboreality, thenthis would support the hypothesis that stabilizingselection had acted to maintain at some level ofarboreal competence.

Abitbol (1995) argued that A. afarensis had a lowsacral promontory angle between its lumbosacraljoint surface and anterior sacral body (70° in AL288-1, compared with his reported range of 44–56°for humans, which I think is a likely underestimateof variability, as I have a human skeleton with anangle of 67°). He argues that this would necessitatehaving their sacrum and pelvis in a more verticalposition than is typical for humans. This differencein sacral angle could be accommodated by the lessanteriorly curved morphology of the sacrum, how-ever, certainly when combined with a lumbar lordo-sis, allowing the lumbosacral joint to lie in the sameplane as that of humans despite the different sacralangle. A. afarensis certainly had a significant lum-bar lordosis, as it has a wide lumbar interfacet dis-tance between the presumed second lumbar andfirst sacral vertebrae (Fig. 4). Increasing interfacetdistances allow the articular processes to imbricate,minimizing the probability of developing spondylol-ysis and spondylolisthesis (Latimer and Ward,1993). Because significant posterior wedging of thevertebral bodies occurs only in the last four lumbarvertebrae (Fig. 4) (Latimer and Ward, 1993), the factthe second lumbar vertebra preserved in AL 288-1 isnot wedged is irrelevant. A lumbar lordosis indicateshabitual upright posture. It even occurs slightly,although to a much lesser degree, in modern nonhu-man primates trained to walk bipedally (Nakat-sukasa, 1991).

Some researchers have proposed that A. afarensisgait was kinematically distinct from that of humans,and that they walked with their hips and knees in amore flexed posture (Susman et al., 1984; Preuschoftand Witte, 1991; Stern, 1999). A bent-knee gait is

unlikely from a kinematic perspective, however, asdemonstrated by Crompton et al. (1998) and Kramerand Eck (2000) using modeling. They demonstratedthat the lower limb length and conformation of AL288-1 would not have produced a less energeticallyefficient gait than in modern humans at walkingspeeds, and Kramer and Eck (2000) even suggestedthey might have even been more efficient. Kramerand Eck (2000) argued that the preferred transitionspeed from walking to running would have beenlower in A. afarensis than in humans. They went onto suggest that this would have affected distance oftravel or day range, although there appears to be noreason to assume any effect on day range based ontheir analysis.

Ruff (1998) and Rak (1991) both argued that theanatomy of AL 288-1 could only be explained if A.afarensis walked with greater pelvic movementsthan do modern humans, although neither of themproposes a bent-hip-and-knee gait. AL 288-1 hasfemoral head dimensions expected for a hominin ofher size (McHenry, 1991; Ruff, 1998), and her fem-oral diaphysis is even stronger. However, because ofthis, coupled with her longer femoral neck, Ruff(1998) suggested that A. afarensis pelvic movementsduring gait would have had to be greater because ofgreater predicted hip and femoral strains. Becausehis analysis of mediolateral bone strength was madein relation to anteroposterior strength, the fact thatA. afarensis seems to have had proportionally stron-ger bones throughout its skeleton (Ruff, 1998; Coff-ing, 1998) could confound his comparison. It is also

Fig. 4. Distance between superior zygapophyseal facet jointsin caudal eight vertebrae of Homo sapiens with 5 and 6 lumbarvertebrae, respectively, Pan troglodytes, Australopithecus africa-nus STS 14, and A. afarensis AL 288-1. All hominins have in-creasing lumbar interfacet distances throughout lumbar skele-ton, but chimpanzees do not. This uniquely hominin trait reflectspresence of a lumbar lordosis, as it allows zygapophyses to slidepast each other when spine is extended, permitting lordotic pos-ture (Latimer and Ward, 1993). Data from Ward and Latimer(1991). Line drawing by Luba Gutz, from Latimer and Ward(1993).


unclear why A. afarensis would have a very largebicondylar angle in this situation. Still, Ruff (1998)did not argue for a bent hip posture. Rak (1991) alsoposited greater pelvic movements, although in pelvicrotation rather than lateral elevation. Neither ofthese situations was modeled by Crompton et al.(1998) or Kramer and Eck (2000), and they bothdiffer from one another. So, although there havebeen main arguments made for a kinematically dis-tinct gait, there is still no consensus on how theirgait differed, or what the costs in energy expendi-ture or mobility would have been.

A bent-knee posture is also inconsistent with thedistal femoral morphology of A. afarensis. The ex-panded calcaneal tuberosity of A. afarensis indicatesthat initial contact during gait was a heel strike (seealso, Gebo, 1996), and that weight was borne on asingle support limb (Latimer and Lovejoy, 1989).Heel strike would have occurred with the knee at ornear full extension, as it in humans, and the kneewould have been straightened further through mid-stance and late stance. The lateral lip of the patellargroove is higher than the medial one in both A.afarensis specimens AL 129-1 and AL 288-1, anddiffers markedly from the situation seen in apes,despite the mediolaterally broad distal femur re-tained in A. afarensis (Fig. 5). AL 288-1 is slightlydamaged along its superior patellar surface, whichoften cannot be appreciated on casts. This elevatedsurface is consistent with the valgus angle, and withsignificant quadriceps muscle contraction at or nearfull extension, as would occur from initial contactthrough early preswing phases of bipedal gait. A.afarensis also exhibits elliptical lateral femoral con-dyles with the flattest region on the distal surface,

as do modern humans (Fig. 5). Even though thedegree of femoral condylar flattening may not be asextensive as in most adult modern humans, theirshape is fully human-like and resembles that ofmodern 10–12-year-old humans (Tardieu, 1998).This morphology serves to increase tibiofemoral ar-ticular contact at or near full extension of the joint,such as occurs in humans during the stereotypicloading patterns of normal gait. Apes have nearlycircular condylar profiles, with similar joint con-tours in all positions in the knee flexion-extensioncycle. This indicates that peak transarticular loadsoccurred at or near full knee extension in A. afaren-sis, rather than in a bent-knee posture, during bipe-dal progression, as in humans. Monkeys have an-teroposteriorly expanded knee joints, but thisresults from a deepening of the patellar surface andminimal overlap between the patellar and tibialjoint surfaces (Fig. 4). The tibial surfaces are re-stricted to a posterior position, reflecting habituallybent knees. Because A. afarensis individuals werehabitual bipeds, if the knee was adapted to beingloaded in partial flexion at heel strike, we should seeeither no flattening, as muscular energy could beused to dissipate ground reaction forces, or else anyflattening should be oriented further posteriorly.

These data do not support the hypothesis that A.afarensis had a lower limb posture appreciably dif-ferent from that of humans during bipedal gait.Data suggesting different distributions of subchon-dral surface at the A. afarensis hip joint (MacLatchy,1996) may reflect the different patterns of musculo-skeletal anatomy surrounding the hip joint ratherthan different limb posture.

Fig. 5. Lateral and inferior views of distal femurs of Pan troglodytes, A. afarensis AL 129-1 (both views), AL 333 (AL 333w-56 aboveand 333-4 below), Homo sapiens, and Theropithecus oswaldi (KNM-ZP 45), a large-bodied fossil cercopithecine from Kenya. Homininsall have anteroposteriorly flattened condyles. T. oswaldi also has elliptical condyles, although without inferior flattening. Below, tibialcontact surfaces are shaded. All hominins have anteriorly expanded condyles, unlike T. oswaldi, whose tibial surfaces are dorsallyrestricted, indicating habitually flexed knee postures. Milder morphology of AL 129-1 compared with larger Hadar specimen andhumans likely represents diminutive size of this specimen, and is in the range for young humans (Tardieu, 1999).


Another feature in which Australopithecus is pre-sumed to have been more chimp-like than are hu-mans is in its talocrural joint. Based on the dimin-utive AL 288-1 talus and tibia, Latimer et al. (1987)reported that the anteroposterior convexity of thetalar trochlea was more tightly curved than is thatof humans or gorillas, matching only chimpanzeesamong extant hominoids. Furthermore, when rangeof joint motion was estimated by articulating theassociated tibia, AL 288-1 had 2–3° greater range ofmotion than seen in humans or gorillas (Stern andSusman, 1983), which they interpreted as advanta-geous for climbing in trees, suggesting arboreality inA. afarensis. A new, larger talus from Hadar, AL147-30 (unpublished findings), has a flatter trochleathan that of AL 288-1, with a subtended angle ofonly 115°, considerably less than that of AL 288-1,which is 140° (Latimer et al., 1987). The new talusfalls within the human range (humans range from95–120°, and chimpanzees from 110–145°. This doesnot necessarily indicate that large and small Hadarhominids differ in locomotor repertoire, becausethese individuals do not exceed the range of varia-tion within extant species. Thus this new fossil re-futes the hypothesis that the talocrural joint wasdistinct from that of extant humans, although thespecies range may have been lower. It is notable thatgorillas have a range of values from 90–120°, likehumans, suggesting an allometric effect (Latimer etal., 1987).

The relatively longer toes of A. afarensis (Sternand Susman, 1983; Susman et al, 1984; White andSuwa, 1987) have been suggested to imply a differ-ent gait pattern. Whether or not the gait of A. afa-rensis would have looked unusual due to havinglarger feet is uncertain. There are no associatedpedal and lower limb skeletons to assess relativefoot length empirically. Further, the variationamong extant humans with different relative footand toe lengths is considered normal intraspecificvariation, and few researchers would argue that anyhumans are more or less effective bipeds as a con-sequence.

In summary, while several researchers have pos-ited a less efficient form of bipedality for A. afaren-sis, none has yet falsified the hypothesis that lowerlimb posture was not within the range of modernhumans. Furthermore, the various analyses fail tosupport a single mechanism by which they differ,instead positing either different hip postures ormovement during locomotion. Data are unclearwhether the ape-like aspects of the A. afarensis skel-eton diminished their efficiency as terrestrial bi-peds. While the detailed kinematic profile of A. afa-rensis individuals might differ in some ways fromthat of humans, there is no certainty that theywould have been less capable bipeds as a conse-quence of their retained primitive traits. This thenbegs the question of why Homo altered the primitivehominin pattern, with its apparent mechanical im-provements for bipedality. There are multiple possi-

bilities, which are largely beyond the scope of thispaper. Increasing body size may have played a part,along with other selective pressures to modify pelvicform to accommodate childbirth for larger-brainedinfants (Tague and Lovejoy, 1986; Ruff, 1998). Atpresent, there is no clear refutation of the hypothe-sis that the primitive traits in the A. afarensis skel-eton compromised their bipedal ability.

Continuing morphological refinement or stasis?

There is actually little fossil evidence to defini-tively answer this question. There is certainly notenough to accurately assess change in patterns ofvariation over time. It appears, however, that thegeneral pattern of postcranial morphology exhibitedwithin Australopithecus was essentially constant.There is little evidence so far to suggest that Aus-tralopithecus morphology continues to change overtime and become more human-like, although it ispossible that there may have been minor modifica-tions of the basic pattern in different species.Broadly speaking, there is an Australopithecus pat-tern of morphology that changes appreciably onlywith the advent of Homo erectus/ergaster around 1.8mya.

Within A. afarensis, the only taxon for which thereis even a hope of assessing temporal change (as incraniodental material; Lockwood et al., 2001), thereis no apparent change over time postcranially. Com-paring earlier and later Hadar specimens, there areno apparent differences in postcranial form (but seeSenut, 1978, but see 1980; Tardieu, 1979, 1986a,b),and certainly none identified so far to be outside therange of variation exhibited in a modern species. Noother Australopithecus species has a sufficient num-ber of specimens or temporal resolution to observepotential change over time.

Across australopithecine taxa, there are onlyweak hints of temporal trends to become less ape-like and more human-like postcranially. The earliestAustralopithecus species identified so far is A. ana-mensis (Leakey et al., 1995, 1998; Ward et al.,1999a, 2001). Postcranially, A. anamensis is knownfrom only the proximal and distal thirds of a tibia, adistal humerus, a nearly complete radius, and acapitate and partial proximal manual phalanx. Inmost ways, these bones closely resemble those of A.afarensis. From the tibia, we can infer that A. ana-mensis was a habitual biped: as in all other homi-nins, the A. anamensis tibia displays a diaphysisthat is oriented normal to the talocrural joint sur-face, rather than the varus angle found in apes (Fig.6) (Latimer et al., 1987; Ward et al., 1999a). Thehumerus, discovered long before it was attributed toA. anamensis (Patterson and Howells, 1967), is in-distinguishable from that of A. afarensis (Feldes-man, 1982; Hill and Ward, 1988; Lague andJungers, 1996; Ward et al., 2001), despite sugges-tions that it is more like that of Homo (Senut andTardieu, 1985; Baker et al., 1998), as is the phalanx.The radius is similar as well, and belonged to a


forearm that was longer than the longest one pre-served for A. afarensis (Heinrich et al., 1993). Thissuggests that the forearms of A. anamensis were atleast as long as those of A. afarensis, and almostassuredly longer for their body size than those ofHomo. The capitate is poorly preserved, but sug-gests a more laterally facing second metacarpalfacet than is seen in any other hominins, and in-stead resembles the condition found in great apes.The only place in which these taxa differ is thecapitate facet, reflecting rotational ability of the sec-ond carpometacarpal joint (Leakey et al., 1998). Be-cause it is likely that A. anamensis and A. afarensisrepresent a single lineage, there is evidence of post-cranial change only in the hand, but that bipedalityhad been established by 4.2 million years ago. Thissuggests that the primitive traits seen in A. afaren-sis probably had been retained by bipedal homininsfor nearly a million years.

A. afarensis and A. africanus are similar postcra-nially in overall morphological pattern, althoughthere are some comparatively minor differences(Hausler, 2001 and references therein). When theydiffer, A. africanus generally has slightly more hu-man-like morphology than does A. afarensis, but not

always. Although their hands are strikingly similarmorphologically, A. africanus appears to have moregracile metacarpal shafts and slightly straighterphalanges with less well-developed flexor ridgesthan does A. afarensis (Ricklan, 1987). There alsoseems to be a large apical tuft on the pollical distalphalanx. Although this bone is not known for A.afarensis, the other A. afarensis distal phalangeshave narrow apical tufts (Bush et al., 1982). The A.africanus pelvis appears to have had a slightly moreanteroposteriorly expanded inlet with a more sagit-tally oriented iliac blades, with better-developed cra-nial angles of the sacrum. This suggests a differentoverall shape of the lower torso in each species.Hausler (2001) reported on an indistinct iliofemoralligament attachment in A. afarensis compared witha distinct one in A. africanus, but given the preva-lence of an intertrochanteric line on the femur in A.afarensis, it seems that this ligament was strong inboth species. Hausler (2001) also showed that thelatissimus dorsi attachment site on the iliac crest ismore medially restricted in A. africanus, like mod-ern humans, than in A. afarensis, suggesting lesspowerful upper limbs in the Sterkfontein hominins.

There are several other ways in which A. africa-nus has been interpreted to be more primitive andarboreal, however. Clarke and Tobias (1995) arguedthat STW 573 had an abductable hallux. Observa-tion of the original specimen reveals that this spec-imen does not differ from A. afarensis or from OH8in joint morphology and orientation, however(Leakey 1960, 1961), which is attributed to Homo/Australopithecus habilis (Leakey et al., 1964). A.africanus also has been suggested to have more ape-like limb proportions than does A. afarensis(McHenry and Berger, 1998), but Hausler (2001)noted that upper limb length to acetabulum sizedoes not differ between two partial skeletons of A.afarensis (Al 288-1) and A. africanus (STW 431).Differences noted by McHenry and Berger (1998) inassociated skeletons reflect the relatively large ra-dial head of A. africanus (Hausler, 2001).

In summary, A. africanus may have been slightlymore derived than was A. afarensis in most featureswhere the species differ. Because A. africanus islater in time (McKee, 1993; Walter, 1994; McKee etal., 1995), this could indicate a directional trend. Ifthese taxa represent a single lineage, this mightsignal disaptation in the traits that change and theirrelated soft tissues.

Australopithecus boisei is too poorly known post-cranially to compare. A. robustus, on the other hand,is known from a number of postcranial bones, al-though many cannot be attributed to Australopithe-cus with certainty, as Homo is also known from thesame sites. The putative A. robustus hand bones aredescribed as more human-like, with broader apicaltufts on the terminal phalanges and flat first meta-carpal bases (Susman, 1988, 1989). Its ilium (SK3155) has been described as having a relativelywider and more cranially extensive iliac blade with a

Fig. 6. Above, posterior views of distal tibias of Homo sapiens,Australopithecus anamensis (KNM-KP 29285), and Pan troglo-dytes, oriented so that talocrural joint surfaces are horizontal.Below, graph of angles of inclination relative to talar surface inextant and fossil taxa (adapted from Latimer et al., 1987). Allhominins have vertically oriented tibial shafts relative to talarjoint surface, whereas apes have sharply inclined tibial shafts,placing knee well lateral to ankle in terrestrial plantigrade pos-ture.


larger auricular surface than those of A. africanusand A. afarensis (Brain et al., 1974; McHenry, 1975),but this variation may reflect body size and/or indi-vidual variation (McHenry, 1975). Other A. robustuspostcranial bones are not notably different fromthose of A. afarensis or other Australopithecus spe-cies (Broom and Robinson, 1949; Napier, 1959, 1964;Robinson, 1970; Day and Scheuer, 1973; Brain et al.,1974; Susman, 1989; McHenry, 1994; Susman et al.,2001). Suggested variation certainly does not ap-proach the condition seen in Homo erectus/ergaster.

No other Australopithecus species is known post-cranially. Postcrania from the Hata Member of theBouri Formation in Ethiopia cannot be definitivelyattributed to A. garhi, the only hominin identified atthe site (Asfaw et al., 1999). However, these fossilsdisplay a primitive, A. afarensis-like brachial indexbut with a proportionately longer lower limb, sug-gesting selection for increased lower limb length ifthis hominin was a descendent of A. afarensis.

Thus, the basic pattern of postcranial anatomyexhibited by A. afarensis appears to persist for over3 million years, suggesting that its locomotor adap-tation was stable, and not undergoing ongoing selec-tion for improved terrestrial competence. The slightdifferences between A. africanus and A. afarensismight signal slight directional selection towards aHomo-like condition if they had an ancestor-descen-dent relationship, which is far from certain. Simi-larly, if the postcrania from the A. garhi site rep-resent a descendent of A. afarensis, lower limbelongation may have occurred. These observationsare speculative, and meant only to point out possi-bilities. If they were eventually supported by furtherevidence, this might support a hypothesis of disap-tation for some primitive traits of A. afarensis.

The length of time over which the basic Australo-pithecus pattern appears to have been retainedseems to be the strongest evidence that primitivemorphology retained an adaptive advantage for Aus-tralopithecus individuals, although it does not fal-sify the null hypothesis of nonaptation. If bipedalitybegan with late Miocene putative hominins like Sa-helanthropus and Orrorin, both about 6 millionyears old, it would have been around for 3 millionyears before the appearance of A. afarensis. Even so,it had been around for almost 1 million years sinceA. anamensis. The general australopithecine bodyplan remains for perhaps up to 1 million years ago,until the disappearance of this species. If the prim-itive Australopithecus traits were disadvantageous,selection would have had ample time to eliminate oralter them. If they were selectively neutral, we needto explain why they never changed until the appear-ance of Homo.

Did A. afarensis actually climb trees?

Another question to address would be whether ornot we have enough evidence to assess whether A.afarensis was actually climbing trees or not. Thiswould be important to reconstruct behavior, and to

perhaps hint at the evolutionary significance of ar-boreality. Relatively few studies have investigatedthis possibility. Data about actual behaviors willcome from traits that are phenotypically plastic, andreflect an individual’s behavior pattern (Churchill,1996; Lieberman, 1997). As noted above, one poten-tial avenue of research is the investigation of diaph-yseal structure in Australopithecus (Ruff, 1998; Ruffet al., 1999), as it is developmentally sensitive.

Because the derived signal for terrestrial bipedal-ity is clear, we can hypothesize that not only had A.afarensis been selected to be bipeds, but that theyactually traveled bipedally. The pronounced femoralbicondylar angle indicates that A. afarensis actuallyengaged in bipedal walking or running (Tardieu andTrinkaus, 1995; Duren, 1999). The flattened femoralcondyles may also reflect habitual loads in kneeextension, as joints appear to be shaped duringgrown by response to hydrostatic pressure in artic-ular cartilage (Frost, 1990a; Hamrick, 1999). Evi-dence for tree-climbing is less clear, but also notthoroughly explored.

Coffing (1998) examined metacarpal diaphysealrobusticity in Australopithecus and extant homi-noids. She argued that skeletal changes improvingterrestrial competence in A. afarensis would havedecreased their arboreal capabilities. She predictedthat if A. afarensis still practiced arboreal behaviors,they would have to have had even greater forelimbstrength than extant apes. She did not explicitlydiscuss issues of genetic vs. epigenetic effects ondiaphyseal form, but given assumptions about bonemodeling, it was implicit that individual behaviorswere involved. Her analyses suggested that A. afa-rensis did indeed have stronger metacarpal diaphy-ses than would be expected for their body size andbone lengths compared with those of modern hu-mans. Ruff (1998) reported that the femur was alsomore robust than humans or apes, however, sug-gesting that their skeletons were more robust over-all than the modern taxa, rather than being tied toarboreality or bipedality. Still, this provides someindirect support for Coffing (1998). Coffing (1998)implied that her hypothesis is mainly about upperlimb strength, but it could be interpreted to meanstrength throughout the body.

Indicators of muscle size and strength in A. afa-rensis tend to be large relative to modern humans,such as deltoid tuberosities (Aiello and Dean, 1990),flexor muscle insertion sites manually and pedally(Marzke, 1983; Stern and Susman, 1983; Susman etal., 1984), and the peroneal groove on the fibula andperoneal trochlea on the calcaneus (Latimer andLovejoy, 1989, 1990b). Indicators of relative muscu-larity in all regions of the A. afarensis skeleton aregenerally greater than in modern humans, as withall premodern hominins (Ruff et al., 1993, 1999;Coffing, 1998). If overall muscularity was greater inA. afarensis than in modern humans, it would not bepossible to test whether this was to improve climb-


ing specifically, or for other reasons such as foragingor defense.

Richmond (1998) and Paciulli (1995) conductedcross-sectional growth studies of phalangeal curva-ture in apes and humans. They both found thatcurvature is greatest during the juvenile period,roughly at the time in which juveniles spend thegreatest proportional amount of time engaging inarboreal behaviors. If their results are confirmed byother analyses, particularly longitudinal ones, thiswould be a character indicating that at least juvenileA. afarensis spent time in the trees. Contrary to theresults of phalangeal studies, Tardieu and Preuschoft(1996) inferred that the morphology of developingepiphyseal plates was affected by behavior, and thatthe immature Hadar femora resemble those of hu-mans, and not apes. This suggested to them that A.afarensis individuals were not climbing, as theylacked the apparent adaptations for stabilizing theepiphysis during arboreality. Duren (2001) alsofound significant links between epiphyseal orienta-tion and form and locomotion among catarrhines.

Another example of a trait that is clearly influ-enced by behavior to at least some degree is humeraltorsion (Martin and Saller, 1959; King et al., 1969;Sarmiento, 1985; Pieper, 1998). As noted above,Australopithecus has less humeral torsion than dohumans or extant great apes. This could be inter-preted as a series of evolutionary reversals or char-acter transformations from an ape-like ancestor toAustralopithecus to human. However, this featuremay well be epigenetically influenced, as captiveand wild orangutans vary in their degree of torsion.It certainly seems to be modified by activity through-out ontogeny in humans (Martin and Saller, 1959;King et al., 1969; Sarmiento, 1985; Pieper, 1988).Handball players (Pieper, 1988) and baseball pitch-ers (King et al., 1969) have higher levels of torsionthan other people. Because humeral torsion also isinfluenced structurally by scapular position and el-bow joint orientation, via whatever mechanisms, thefact that A. afarensis differs from humans and ex-tant apes in having less torsion could be related tothe inferred different shape of their thorax (Schmid,1983; Jellema et al., 1993). Thus, lower humeraltorsion in A. afarensis could represent structuraldifferences resulting from selection for torso shape,from different upper limb use, or both. These possi-bilities warrant further investigation.

Finally, when assessing the likely behaviors ofAustralopithecus, we can consider the capabilitiesevident in their morphology. Even if A. afarensisspent time in the trees, without a grasping hallux(White and Suwa, 1987; Latimer and Lovejoy,1990b; but see Clarke and Tobias, 1995) they wouldhave been significantly less agile than are apes andmonkeys, especially in the case of females holdinginfants. Despite the apparently slightly longer andmore curved toes than are typical for modern hu-mans, their toes were still shorter and straighterthan those of apes (Bush et al., 1982; Latimer and

Lovejoy, 1990b; Stern and Susman, 1983; White andSuwa, 1987), and so the size of supports they couldhave grasped would be less. Even if their manualgrasp was greater than that of humans, and theirpedal grasp like that of the manual grasp of modern2-year-old humans (Susman et al., 1984; Stern,2000), we still cannot be sure that this was retainedfor adaptively significant arboreal behaviors. Theywould have been more competent in the trees thanare typical humans, as they are much stronger andhad very slightly better mechanics with longerarms, fingers, and toes. Any arboreal locomotionwould still necessarily have been fairly slow anddeliberate, however, more for something like sleep-ing in trees than for hunting or fleeing from preda-tors. Certainly females with infants would have haddifficulty climbing trees, because without graspinghalluces they would have had to hold onto theirinfant with at least one arm. Still, sleeping in treesfor safety is a potentially significant behavior that,at least in theory, could have selected for some rel-atively weak climbing capabilities.

In summary, studies of ontogenetically sensitivemorphology have shown that A. afarensis individu-als walked bipedally, but do not lead to a consensusabout A. afarensis locomotion. Relatively few studieshave been conducted so far, however. Research onthe influences of individual activity patterns on thedevelopment of adult morphology is key to determin-ing what behaviors A. afarensis individuals engagedin over the course of their lifetime, and are wellworth pursuing.

THE MANY INFLUENCES ON MORPHOLOGY

When using morphological features to make phy-logenetic or behavioral inferences about fossil taxa,we need to keep in mind the integrated nature ofanatomy (recent discussions in Witmer, 1995;Churchill, 1996; Lieberman, 1997, 1999; Lovejoy etal., 1999, 2000). Of course, though all we have arethe bones of fossil animals, we need to bear in mindthat the growth and function of soft tissues caninfluence skeletal form (Witmer, 1995, 1997). Weknow that activity pattern can affect bone shape(e.g., Arkin and Katz, 1956; Carter and Wong, 1988;Ruff, 1992; Ruff et al., 1993, 1994; Trinkaus et al.,1991, 1994; Tardieu and Trinkaus, 1994; Churchill,1996; Martin et al., 1998; Skerry, 2000), as can se-lection on soft tissues (e.g., Gibbs et al., 2002; Wit-mer, 1995, 1997). We also know there may be geneticand other developmental links among structures(e.g., Zelditch, 1987, 1988; Alberch, 1982; Cheverud,1984; Maynard Smith et al., 1985; Lieberman, 1997,1999; Hall, 1999; Tardieu, 1999), so that selectionfor an aspect of one trait can directly impact theform of another. This is not to say, however, thatselection cannot independently modify structures,only that it is possible that structures may experi-ence modifications concomitant with selection on alinked trait. The functional and evolutionary signif-icance of bone form can only be understood accu-


rately if the range of influences on it is elucidated.The existence of these effects and their potentialconsequences is not a new revelation, but has al-ways been verging on unobtainable information, andso by practical necessity is often ignored.

An example of integrated morphology is the shiftin overall torso shape in apes and monkeys (Benton,1965, 1976; Ward, 1991, 1993). Great apes havevertebral transverse processes that arise from theneural arch rather than the vertebral body, flaringiliac blades, and coronally oriented scapulae, alongwith concomitant shifts in related muscular anat-omy. Rather than positing that each of these fea-tures was under independent selective pressure, be-cause they are spatially and structurally relatedwith one another, and always correlated, they ap-pear to represent related changes resulting from areorganization of the torso, in this case to enhancethe effectiveness of abduction-adduction movementsof the arm for arm-hanging and forelimb-dominatedarboreal activities.

Recent scientific progress is improving our abilityto incorporate pleiotropic and ontogenetic informa-tion in paleontological interpretations. Discoveriesin the fields of genetics and developmental biologyhave been rapidly increasing our knowledge aboutthe control and ontogenetic mechanisms of structureformation (e.g., Hinchcliffe, 1991; Wolpert, 1983;Hall, 1999; Cohn and Bright, 2000; Gilbert, 2000;Skerry, 2000; Hamrick, 2002; other articles inO’Higgens and Cohn, 2000). An interesting set ofexamples of developmental genetic links among ap-pendicular and axial structures comes from studiesof Hox genes, as well as other gene systems such asPax. Alterations in their expression appear to affectthe condensation and proliferation of limb-bud mes-enchyme, and mutations in these genes generallyhave multiple effects on the resulting skeleton(Davis and Capecchi, 1994; Favier et al., 1995, 1996;Fromental-Ramain et al., 1996). Such links can pro-vide mechanisms whereby selection on one aspect of

the skeleton can result in changes elsewhere (Tague,2002a). For example, a combination of Hoxa-11 andHoxa-13 mutations can result in reduction of thefirst ray and increased length of rays 2–5, mirroringchanges thought to have occurred in apes. Hoxd-11can be responsible for a suite of alterations, includ-ing reduced metacarpals 2–5, reduction of the ulnarstyloid process, and transformation of a sacral ver-tebra into a lumbar one (Davis and Capecchi, 1994;Favier et al., 1995, 1996). A broadly similar suite ofmorphologies appears to differentiate homininsfrom apes, suggesting the possibility of a single ge-netic change resulting in multiple developmentalshifts. The extent to which a single gene is involvedremains to be determined, but pleiotropy is a tena-ble hypothesis. As the details of these links and theireffects on adult form continue to be worked out, it iscritical that we incorporate this type of informationinto our morphological and phylogenetic interpreta-tions.

The most explicit attempt to assess and code thetypes of interaction among tissues and structuresvia ontogeny and selection in determining form hasbeen that of Lovejoy et al. (1999, 2000). They pro-posed five trait types that differ in the degree towhich they are acted upon directly or indirectly byselection, are influenced by selection on relatedstructures, or are epigenetically influenced by indi-vidual activity over a lifetime (Table 1). This classi-fication system represents a model to employ whenattempting to interpret evolutionary history or be-havior in fossil taxa, and so should be useful forassessing Australopithecus. By employing eitherthis system, or at least the logic underlying it, weshould be in a better position to more accuratelyinterpret early hominin morphology.

The difficulty will often be in identifying the spe-cific influences on a trait, and classifying individualtraits, as illustrated by some of the examples inLovejoy et al. (1999, 2000). In addition, some char-acters may fall into more than one type category,

TABLE 1. Analytical trait types proposed by Lovejoy et al. (1999, 2001)

Trait type 1: A trait that differs in two taxa because its presence and/or expression are downstream consequences of significantdifferences in the positional information of its cells, and their resultant effects on pattern formation. Type 1 traits are fixed bydirectional and/or stabilizing selection because their primary functional features have a real effect on fitness, and result largelyfrom a direct interaction between genes expressed during tertiary field deployment and the functional biology of their adultproduct.

Trait type 2: A trait which is a collateral consequence of changes in positional fields which are naturally selected (type 1), i.e.,they are byproducts of field changes whose principal morphological consequences provide significant functional benefits to theirphenotype. Type 2 traits differ in two taxa because of differences in pattern formation (as in type 1), but their functional effectis so minimal as to have had no probable real interaction with natural selection. Their principal difference from types 4 and 5is that they represent true field-derived pleiotropy.

Trait type 3: A trait that differs in two taxa because of modification of a systemic growth factor that affects multiple elements,such as an anabolic steroid.

Trait type 4: A trait that differs between taxa and/or members of the same taxon because its presence/absence and/or “grade” areattributable exclusively to phenotypic effects of the interaction of connective tissue “assembly rules” and mechanical stimuli.Such traits have no antecedent differences in pattern formation, and therefore have no value in phyletic analysis. They areepiphenetic and not pleiotropic. However, they provide significant behavioral information, and are of expository or evidentiaryvalue in interpreting fossils. They often result from habitual behaviors during development and/or adulthood.

Trait type 5: Traits arising by the same process as those of type 4 but which have no reliable diagnostic value with respect tobehavior. Such traits are not consistently expressed within species, and often show marked variation of expression withinindividuals and local populations.


having multiple influences, and so perhaps sendingus multiple signals. Still, using this general ap-proach, we can construct testable hypotheses aboutthe functional and evolutionary relevance of charac-ters, and test them using experimental approaches.Such tests might arise using locomotor studies, de-velopmental genetic and molecular biology, or thecomparative method. The importance of this schemelies in its attempt to identify the influences on boneform.

An excellent example of a trait whose influencescurrently are under intense scrutiny is long bonediaphyseal form. One bone mechanical theory statesthat certain levels of strain trigger bone-modelingresponses, as bone models to maintain particularstrain distributions necessary to perform necessarymetabolic function while maintaining structural in-tegrity (Martin et al., 1998 and references therein).Using engineering beam theory, investigators haveinferred that because bones are subjected to bendingunder normal physiological loading conditions, thegreatest tensile strain caused by bending should belocated near midshaft. Tensile strain is thought toinvoke the most significant modeling response inbone. Operating on the assumption that bone mod-els to minimize tissue strain, researchers inferredthat the plane in which maximum bending occursshould have the greatest bending rigidity. Thus, theamount of load to which a bone is subjected duringgrowth should be reflected in its midshaft diaphy-seal cross-sectional geometry. This assumption wasused to infer activity patterns in humans and otherprimates (Ruff, 2000; Martin et al., 1998).

As this field of inquiry developed, it was graduallyrealized that other variables such as body shape areinfluential in determining long bone form. It cer-tainly is becoming apparent that there is an ageeffect on the responsiveness of bone to activity pat-tern, because mechanical sensitivity of the modelingresponse appears to diminish as an individual ap-proaches skeletal maturity (Frost, 1990a, b; Carterand Beaupre, 2001). Furthermore, some experimen-tal strain gauge work suggests that contrary to theassumptions used to infer habitual direction ofbending strain in long bones, the plane of greatestbending rigidity may not always be the same as theplane of greatest bending strain, at least duringloads incurred by walking or climbing (Demes et al.,1998, 2001). It may be that patterns of muscle re-cruitment, when counteracting ground reactionforces, may exert more relevant strain distributionsrather than simply the ground reaction vectors.However, the one animal that galloped in the study,incurring maximum strain values, did have peakstrains that approached the orientation predicted bybone sectional form (Demes et al., 2001). This maysuggest that it is the peak strains only that stimu-late diaphyseal modeling to improve bending rigid-ity near bone midshafts, altering their shapes.

These studies point to our need for caution whenusing cross-sectional diaphyseal form to infer behav-

ior. They also suggest that different bones have dif-ferent constraints on their form. Most recently, itwas proposed that epiphyseal plate form is a greaterdeterminant of diaphyseal cross-sectional form thanis activity (Ohman and Lovejoy, 2001). Data sug-gest, however, that while within some taxa theremay be an effect of epiphyseal geometry on diaphy-seal midshaft shape, there is considerable variationin this relationship, and it does not hold true withinor among taxa in metacarpals (Holden and Ward,unpublished data) or femur (Nalley and Ward, un-published data). It appears now that there may bean inherent, genetically influenced initial shape de-termined in part by selection on joint form, whichinfluences epiphyseal geometry. This geometry mayhave a slight effect in diaphyseal cross-sectionalform. This initial form then may be modified byactivity pattern (Martin et al., 1998 and referencestherein), especially early in life (Ruff et al., 1994).Body proportions and muscle distributions about thebone affect patterns of bone strain, and ultimatelydiaphyseal form. It also appears that bone may notmodel to eliminate strain, but to enhance predict-ability of strain, and even to maintain a certain levelof strain with activity (Bertram and Biewener, 1983;Rubin, 1984). According to the scheme of Lovejoy etal. (1999, 2000) (Table 1), long bone diaphyseal formappears to be a mixture of trait types 1, 2, and 4.

The picture is complex, but this attention to thedeterminants of diaphyseal form is exactly what isneeded to determine the genetic and epigenetic in-fluences on bony morphology, and any other ontoge-netic or pleiotropic effects. Armed with such detailedinformation, we will be better able to accuratelyinfer activity patterns from the skeleton. We willalso be in a better position to use morphologicalinformation to infer phylogeny and interpret pat-terns of character transformation within a lineage.

Again, advances in our understanding of geneticand other molecular influences on the developmentof adult form will help us develop and test more suchhypotheses, and improve the accuracy with whichwe interpret the fossil record.

IMPLICATIONS FOR TESTING HYPOTHESESABOUT WHY HOMININ BIPEDALITY EVOLVED

If we want to understand how humans evolved,the operative question is finding out why our earli-est relatives evolved as they did. All of our work todetermine what A. afarensis individuals looked likeand what they did, and how they evolved over time,provides the raw data with which to test hypothesesabout relationships between locomotion and otheraspects of a species’ biology, such as diet or socialbehavior.

Since many hypotheses proposed to explain theevolution of bipedality revolve around diet and foodacquisition (Du Brul, 1962; Hunt, 1994; Jolly, 1970;Prost, 1980; Wrangham, 1980; others summarizedby Rose, 1991; Richmond et al., 2001), it is worthconsidering links between the adoption of Australo-


pithecus bipedality and evidence of diet. A. anamen-sis exhibits different dentognathic morphologiesfrom those of earlier hominoids, and so appears tohave had a different dietary specialization. A. ana-mensis shares thick enamel on its teeth with alllater hominins. It has a reduced anterior dentition.Although not quite as much as seen in later homi-nins, it is considerably more than in any earlier ape.Its mandibular corpus was also not much strongerthan that of apes, and less robust that that of laterhominins (Teaford and Ungar, 2000). Its jaw struc-ture was more ape-like than that of later hominins,however, with nearly parallel postcanine tooth rows,and a deep and receding mandibular symphysis,although the structure of the symphysis differsslightly from that of apes. Thus there appear to bechanges in diet associated with Australopithecus,and thus far, with committed bipedality. Teafordand Ungar (2000) interpreted the A. anamensis mor-phology as signaling a shift in emphasis from soft,tough fruits to hard-object feeding.

If dietary and locomotor changes were necessarilydependent on one another in some fashion, we mightexpect to see them associated in some consistentpattern across bipedal hominins. While there appearto be concomitant dietary and locomotor changesassociated with the origin of Australopithecus, thereis no such evidence within the genus. The evidenceis extremely sparse from which to make such assess-ments with any confidence so far. Still, from whatlittle is preserved, evidence of dietary diversityamong Australopithecus species does not, so far, ap-pear to be associated with a consistent pattern oflocomotor specializations. A. africanus had slightlylarger molars and reduced facial prognathism com-pared with A. afarensis, suggesting continued spe-cialization for hard object feeding (Teaford and Un-gar, 2000). A. africanus may have been even morehuman-like than A. afarensis in some features, al-though there is little overall difference.

A. garhi had large molars like those of robustaustralopithecines, a large sagittal keel, and otherintense chewing adaptations (Asfaw et al., 1999). Ifthe postcranial elements from the same site areindeed those of A. garhi, it would appear to differfrom other Australopitheci postcranially as well,with more human-like limb proportions than theother species for which this can be determined. Theonly associated A. boisei postcranial fossil associatedwith cranial remains is KNM-ER 1500. This fossil ispoorly preserved, but may have had more human-like limb proportions than did A. afarensis (Leakey,1973; Day et al., 1976; Leakey and Leakey, 1978;Grausz et al., 1988). This appears similar to A.garhi, and may suggest a link between hard-objectfeeding specialization and more human-like propor-tions. A. robustus, however, shows only slight evi-dence for such an association. Since all postcraniaattributed to A. robustus are isolated, proportionsare difficult to assess. Two ulnae are unassociatedwith any craniodental material, but have been ten-

tatively referred to robust Australopithecus: OmoL40-19 (Howell and Wood, 1974; McHenry, 1976;Day, 1978; Feldesman, 1979; McHenry and Te-merin, 1979) and Olduvai OH 36 (Walker andLeakey, 1993; Aiello et al., 1999). They appear morecurved than do those of A. afarensis and A. africa-nus, or of those of Homo, and their proximal endsalso have some ape-like characteristics (Drapeau,2001). It is not yet clear, however, whether the hy-pothesis can be falsified that the variation exhibitedby all Australopithecus ulnae exceeds that found inany single extant species, much less genus.

In summary, the heavy chewing adaptations seenin A. garhi and other robust Australopithecus spec-imens do not appear to be systematically linked withmore human-like skeletons, although there may be aslight association. Admittedly, postcranial fossilsare poorly known for most Australopithecus species.As more are discovered, this picture may change. Atpresent, however, while dietary adaptation may wellhave accompanied the origin of Australopithecus,from the limited data available, diet does not appearto be an exclusive correlate of locomotor adaptationamong early hominins. Because of the poor fossilrecord of postcranial anatomy of most Australopithe-cus species, any such conclusions must remain ten-tative at present.

Other hypotheses suggest that social behavior islinked with the acquisition of terrestrial bipedality(Lovejoy, 1981; Jablonski and Chaplin, 1993; otherssummarized by Rose, 1991). One way in which socialbehavior can be reflected in the fossil record is insexual dimorphism. While it is true that Australo-pithecus lost significant canine size dimorphism,they retained a nearly 100% body size dimorphism.Males were almost double the size of females(McHenry, 1991, 1992, 1994), as evidenced by highlevels of sizes represented in all species of Australo-pithecus for which this is measurable (reviewed inPlavcan, 2000, 2001). No monogamous extant pri-mate species has this much size dimorphism. Allextant taxa with this much body size dimorphismare polygynous, either living in single- or multimalegroups, but with fairly intense levels of male-malecompetition (Plavcan, 2000, 2001). Hence, while it isclear that relatively large canines had ceased toconfer reproductive advantage to male hominins,body size was apparently still valuable. Thus, thedata do not support an association between monog-amy and bipedality. The data do offer a link betweenthe cessation of canines as useful weapons in male-male competition and the origins of committed bipe-dality, however. Furthermore, this extreme bodysize dimorphism differs from the pattern seen inhumans and Pan, which all have much lower levelsof body mass dimorphism. Pan retains significantcanine dimorphism, while humans do not. The datasuggest that Australopithecus social systems dif-fered from those seen in chimpanzes, bonobos, orhumans. Similarities in social behavior shared be-tween humans and chimpanzees on the one hand


(Wrangham, 1999), and humans and bonobos on theother (Zihlman et al., 1978), appear to have evolvedindependently.

The nature of early hominin bipedality, and ofpotential arboreal competence, bears on other be-havioral reconstructions of early hominins. Chim-panzee-like hunting would not be possible for Aus-tralopithecus, given their anatomical adaptations tobipedality, even if they did use trees to some extent,because it relies on a high level of arboreal compe-tence. Thus, the importance of hunting for chimpan-zees and humans (Stanford, 2001) appears to havebeen acquired independently.

Other hypotheses about early hominin behavior,of which there are many, are not directly testableusing data from the early hominin record at present,but rely on other lines of evidence. Again, Ardipithe-cus, Orrorin, and Sahelanthropus will provide criti-cal new information for testing hypotheses about theorigins of bipedality by providing potentially newassociations between locomotor, dietary, and socialbehavioral adaptations in early hominins. They willalso provide important information on the directionof morphological change in all regions of the skele-ton, allowing us to assess the evolution and coevo-lution of adaptive complexes in early hominins.

SUMMARY AND CONCLUSIONS

It is always the case that while fossils are the dataon hominin evolution, our theoretical approachesgovern how we interpret them. The debate over lo-comotion in Australopithecus as it has been framedso far is becoming ineffective for helping us under-stand early hominin locomotor evolution. By identi-fying the causes of this debate and reframing thequestions we ask of the fossils, we are in a betterposition to make progress. Some researchers havebeen concerned with attempting to reconstruct theselective regime that shaped A. afarensis, or why itevolved as it did. Others have been more concernedwith reconstructing individual activity patterns, orwhat they were like. Both approaches have value fordeveloping a more complete understanding of theearly radiations of hominins. We also need to remainaware that some details about both research ques-tions will be beyond the limit of resolution allowedby the fossil record.

By clearly acknowledging the questions we areasking about the fossils, we can then use the dataavailable to develop tests of hypotheses about adap-tation and/or behavior. Studies of adaptation muststart with a reliable phylogeny incorporating livingand fossil hominoids. From this, vectors of morpho-logical change can be identified, and with accompa-nying biomechanical and comparative analyses, se-lective regimes can be interpreted. To test whetherprimitive retentions were retained by stabilizing se-lection for maintenance of an ancestral behavior,like climbing trees, we must determine whether theprimitive morphology compromised the derived

function. If this is not possible, we can try to useevidence of stasis or reconstructed behaviors to giveus hints about the extent of stabilizing selection.Disaptation can be disproven by the continuedmaintenance or enhancement of a structure. To testhypotheses about which behaviors A. afarensis indi-viduals engaged in, we can consider the selectiveregime suggested by their apomorphic morphology,but we also must attempt to identify traits that areepigenetically sensitive to activity patterns.

Using this investigative framework, what we caninfer about the selective regime acting on A. afaren-sis at this point is that the immediate ancestors of A.afarensis, and probably A. anamensis and A. africa-nus, had undergone intensive selective pressures tobe habitual terrestrial bipeds. This hypothesis issupported by the numerous derived skeletal modifi-cations from the likely ancestral condition. Mechan-ical analyses suggest that these traits enhanced bi-pedal locomotion, and that they are similar tomodern hominin bipeds. Furthermore, epigeneti-cally sensitive traits, such as femoral bicondylarangles and epiphyseal contours, indicate that A. afa-rensis actively engaged in bipedal locomotor behav-iors. Arboreal competence was reduced, indicatingthat arboreality was of diminished importance forindividual survival and reproductive success. Mostadaptations for arboreality likely present in the lastcommon ancestor of apes and humans were alteredor lost. None was enhanced in response to changesfavoring bipedality, except perhaps for an increaseon overall strength (Coffing, 1998). Clearly, the re-productive consequences of habitual bipedal travelwere considerable.

Moreover, the massive rearrangement of bone andjoint morphology and orientation implies that sub-stantial loads were incurred while traveling bipe-dally. Extant apes are capable facultative bipeds,being able to travel short distances during food-gathering episodes on two feet (Hunt, 1994). Theirability to climb trees is more important to them interms of reproductive success, however, so apes havenot been selected to modify their skeletons to be-come better bipeds. The selective consequences ofproblems that might stem from a musculoskeletalsystem poorly designed for bipedality, such as backproblems or joint pain, are minimal in very short-distance locomotor bouts. On the other hand, thefitness of an animal traveling longer distances moreregularly, at high speed, or for particularly repro-ductively valuable reasons (e.g., inter- or intraspe-cific competition, or carrying), would be in jeopardywith any such maladies. For this reason, the onlyscenario that would select for the major alterationshominins underwent is if bipedality was employedfor more than simply standing and feeding, or walk-ing very short distances. The adaptive importance ofbipedal travel is highlighted by the loss of the manyadvantages of arboreal traits, in particular a grasp-ing hallux, for use in climbing trees with speed and


agility for feeding, hunting, or predator escape, orfor infants being able to cling to their mothers’ fur.

This is not to say that using trees to some extentwas not necessarily selectively valuable for A. afa-rensis, but this assumption is difficult to test. It isalmost certain that A. afarensis individuals wouldhave been more capable climbers than are mostmodern humans. They were smaller and relativelystronger. They retained primitive features, such asslightly longer arms, hands, and feet, that wouldhave made them slightly more competent in thetrees than are modern humans, but still consider-ably less so than any ape. The issue is whether ornot these features were actively maintained forclimbing by causing individuals who lacked them, orin whom they were more poorly developed, to leavefewer descendents than those who did. Particularlyin light of the strong directional signal away fromarboreality towards bipedality, it is difficult to dis-prove the null hypothesis that these traits remainedas secondary nonaptations. There is no conclusiveevidence yet that the retained features of Australo-pithecus compromised its effectiveness as a biped,but many researchers support this idea. The shapeof the femoral condyles and the bicondylar angle donot support the hypothesis that Australopithecuswalked with a bent knee and hip, a position furthersupported by modeling.

The strongest support for a hypothesis of stabiliz-ing selection at the moment is the apparently longperiod over which the Australopithecus suite of fea-tures remained with little apparent modification.Certainly with the appearance of Homo erectus/er-gaster, the hominin postcranial skeleton and proba-bly muscular system underwent significant changes.Before this time, however, despite an increasing dis-cussion of postcranial variation among Australo-pithecus species, there seems to be only a hint of aslight trend toward more “human-like” anatomyover time prior to 1.8 million years ago, and eventhis is a very tentative observation.

What we can say about the behavior of A. afaren-sis is that they were habitual bipeds, based on traitpolarities and epigenetically sensitive traits influ-enced by behavior, such as femoral bicondylar angle.Behavioral indicators of arboreality are unclear.Studies of phalangeal curvature may hint at tree-climbing behavior, but more research is needed tosupport or refute this hypothesis. The robusticity oftheir skeletons may also prove to be related to arbo-real behaviors, but this has not been clearly demon-strated yet. Studies of kinematic characteristics ofA. afarensis gait patterns have produced conflictingresults. Continued elucidation of the genetic, devel-opmental, and epigenetic bases for morphologicalfeatures and character complexes will be of criticalimportance in testing hypotheses about the actualday-to-day behaviors of Australopithecus individu-als. This will also help us explore the current uses towhich primitive traits of A. afarensis were put. Inaddition, these data will help us make more accu-

rate phylogenetic reconstructions by allowing us tomake more appropriate character choices for ouranalyses.

The extent to which A. afarensis was arboreal hasimplications for interpreting the pattern of naturalselection that shaped the early part of our lineage.Recent claims for locomotor diversity among earlyhominin species (Berger and Tobias, 1996; Clarkeand Tobias, 1995; McHenry and Berger, 1998) andthe recovery of new, earlier fossils (White et al.,1994; Haile-Selassie, 2001; Senut et al., 2001; Bru-net et al., 2002) underscore the importance of find-ing ways to more precisely interpret early homininpositional behaviors. In addition, our understandingof Australopithecus locomotor behavior is importantfor understanding the transition to Homo. If austra-lopithecines and other early hominins were partlyarboreal, postcranial changes seen in Homo erectus/ergaster might be due to a shift towards full bipedal-ity. On the other hand, if the ancestors of Homo werealready fully bipedal, the changes in the Homo skel-eton must have been due to other factors, such as anincrease in efficiency due to walking longer dis-tances or running, and/or selection for body size,throwing, tool use, and transport, or any number ofother possibilities. Until we find a way to resolvethis ongoing debate over the importance of arbore-ality in A. afarensis and other early hominins, wewill have a difficult time characterizing the impor-tant transition (or transitions) involving postcranialanatomy that shaped our lineage.

ACKNOWLEDGMENTS

I thank Dave Begun, Mark Collard, Deborah Cun-ningham, Michelle Drapeau, Mark Flinn, AnneHolden, Amy Judd, Bill Kimbel, Bruce Latimer, Thi-erra Nalley, Jason Organ, Brian Richmond, andAlan Walker for helpful discussions about the con-cepts in this paper and sharing information. I thankLee Berger, Ron Clarke, Don Johanson, Bill Kimbel,Bruce Latimer, Meave Leakey, Steve Leigh, BrianRichmond, Philip Tobias, and the staffs of the Cleve-land Museum of Natural History, National Muse-ums of Kenya, the Transvaal Museum, NationalMuseums of Ethiopia, the University of the Witswa-tersrand, and the Institute of Human Origins foraccess to fossil, comparative skeletal, and cadaverspecimens. I also thank Chris Ruff for inviting me tocontribute this manuscript, and Martin Hausler,Dan Lieberman, Henry McHenry, Chris Ruff, andan anonymous reviewer for helpful comments andsuggestions.

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