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

Interpreting the Posture and Locomotion of

Australopithecus 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 interpreting
locomotion in all early hominins. While most researchers
agree 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 being
reduced, 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, while
others are interested in reconstructing A. afarensis behav-
ior. By explicitly outlining whether we are interested in
reconstructing selective history or behavior, we can de-
velop testable hypotheses to govern our investigations of
the fossils. To infer the selective history that shaped a
taxon, we must first consider character polarity. Derived
traits that enhance a particular function, are found to be
associated with that function in extant homologs, and that
epigenetically sensitive data indicate were actually being
used for that function, can be interpreted as adaptations.
The null hypothesis to explain the retention of primitive
traits is that of selective neutrality, or nonaptation. Dis-
proving this requires demonstration of active stabilizing
or negative selection (disaptation). Stabilizing selection
can 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 no
change in variability in the trait are evidence that can
support a hypothesis of adaptation for primitive traits, but
still do not falsify the null hypothesis. Disaptation, or
negative selection, should result in a trait being reduced
or lost. To infer the behaviors of a fossil species, we must
first determine its adaptations, use this to make hypoth-
eses about its behavior, and test these hypotheses using
epigenetically sensitive traits that are modified by an
individual’s activity pattern. When the A. afarensis data
are evaluated using this framework, it is clear that these
hominins had undergone selection for habitual bipedality,
but the null hypothesis of nonaptation to explain the re-
tention of primitive, ape-like characters cannot be falsified
at 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 behaviors
during ontogeny shows that A. afarensis individuals were
habitually traveling bipedally, but evidence presented for
arboreal behavior so far is not conclusive. By clearly iden-
tifying the questions we are asking about early hominin
fossils, refining our knowledge about character polarities,
and elucidating the factors influencing morphology, we
will 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.
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 Swallow
Hall, University of Missouri, Columbia, MO 65211.
E-mail: WardCV@missouri.edu
DOI 10.1002/ajpa.10185
Published online in Wiley InterScience (www.interscience.wiley.
com).

TABLE OF CONTENTS

Introduction ............................................................................................................................................................. 186

Current Hypotheses of Australopithecus afarensis Locomotor Behavior ........................................................... 187
Reasons for the Debate ........................................................................................................................................... 188
Empirical Frameworks ........................................................................................................................................... 189
Hypotheses about adaptation ............................................................................................................................. 189
Hypotheses about behavior ................................................................................................................................. 192

© 2002 WILEY-LISS, INC.

186 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 45, 2002
Reexamination of the Fossil Evidence Using This Framework .......................................................................... 192
Character polarities and vectors of morphological change in early hominins ................................................ 192
Do the derived traits of A. afarensis reflect bipedality? ................................................................................... 197
Did primitive traits compromise bipedality? ..................................................................................................... 197
Continuing morphological refinement or stasis? ............................................................................................... 200
Did A. afarensis actually climb trees? ............................................................................................................... 202
The Many Influences on Morphology .................................................................................................................... 203
Implications for Testing Hypotheses About Why Hominin Bipedality Evolved ................................................ 205
Summary and Conclusions ..................................................................................................................................... 207
Acknowledgments .................................................................................................................................................... 208
Literature Cited ...................................................................................................................................................... 208

INTRODUCTION The debate over hominin locomotion became in-

Bipedality is the hallmark of the human lineage.
Whether or not our unique locomotor mode evolved
in the original members of our clade, it represents a
fundamental adaptive shift away from the apes. Bi-
pedality has served as a significant preadaptation to
the acquisition of other key human characteristics,
such as tool-making, altriciality of infants, and ar-
guably even intelligence. Understanding the nature
and timing of the transition to terrestrial bipedal
locomotion is key to an accurate interpretation of
how and why humans evolved.
Over the past 78 years, our knowledge of the na-
ture of early hominin (which I define as members of
the human clade more closely related to us than to
Pan; see Richmond et al., 2001) bipedality has im-
proved dramatically. Dart (1925) correctly inferred
that the Taung child had upright posture, and that
bipedality characterized the earliest part of the hu-
man lineage. This interpretation was bolstered by
further early hominin fossil finds, particularly in
South 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 and
more numerous Australopithecus afarensis1 fossils
in the 1970s (Taieb et al., 1974, 1975; Johanson et
al., 1982b and references therein) and footprints at
Laetoli (Leakey and Hay, 1979), research on Austra-
lopithecus locomotion intensified, and more detailed
questions began to be asked about the functional
morphology of these hominins.
1
Some 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 and
placed 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 hominin
species originally attributed to Australopithecus (except Ardipithecus
ramidus) as a single genus, and focus my discussions on functional
interpretation of the fossils.
tense in the early 1980s, after the publication of the
Hadar fossil descriptions, and it continues to this
day. Some researchers have presented data support-
ing the hypothesis that Australopithecus afarensis
individuals 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 bipedal
progression stemming from these retained arboreal
characters (Susman et al., 1984; Preuschoft and
Witte, 1991; Rak, 1991; Cartmill and Schmitt, 1996;
MacLatchy, 1996; Schmitt et al., 1996, 1999; Ruff,
1998; Stern, 1999). At least one researcher argued
that A. afarensis was not bipedal at all, but was a
palmigrade-plantigrade quadruped (Sarmiento,
1987, 1994, 1998). The debate is polarized and po-
larizing, and is to the point that it impedes our
further understanding of the posture and locomotion
of early hominins. It serves little further purpose as
it has been framed thus far.
Recently, even earlier hominins have been discov-
ered. Australopithecus anamensis is now known to
have been a committed biped at 4.2 mya, but is
poorly known postcranially (Leakey et al., 1995,
1998; Ward et al., 1999a, 2001). Putative hominins
Sahelanthropus tchadensis (Brunet et al., 2002) ex-
isted 6 –7 mya, Orrorin tugenensis about 6 mya (Se-
nut et al., 2001), and Ardipithecus ramidus from
5.8 – 4.4 mya (White et al., 1994, 1995; Haile-
Selassie, 2001). From the limited data published so
far, the nature of these hominins’ locomotor adapta-
tions cannot be fully ascertained. Regardless of what
we learn about Sahelanthropus, Orrorin, and Ar-
dipithecus in the coming years, Australopithecus,
and in particular A. afarensis, will remain the basis
for our understanding of the origins and early evo-
lution of hominin locomotion. It is the model to
Ward] INTERPRETING A. AFARENSIS LOCOMOTION
which we will compare the new fossils in order to
assess the trajectory of early hominin locomotion,
and is central to our understanding of early hominin
evolution. So, resolving the debate over its locomotor
behavior, and its biology, is still a critical concern of
paleoanthropology.
CURRENT HYPOTHESES OF
AUSTRALOPITHECUS AFARENSIS
LOCOMOTOR BEHAVIOR
The first of three hypotheses suggests that A.
afarensis individuals were palmigrade-plantigrade
quadrupeds (Sarmiento, 1987, 1994, 1998). This
idea is based primarily on a suite of morphological
similarities between the hands and feet of A. afaren-
sis and gorillas, in particular lowland gorillas, which
Sarmiento (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 fingers
and toes than typical for other great apes, a similar
morphology of the hamate-triquetral facet, a more
palmarly directed hamulus and pisiform, broad tib-
ialis posterior insertion, and large plantar aponeu-
rosis (Sarmiento, 1994).
While these similarities might seem to support
this hypothesis, the overwhelming suite of skeletal
modifications 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 neck
structure and condyle shape (Lovejoy et al., 1973;
Johanson et al., 1982a), are not shared with gorillas,
and do not support the hypothesis of quadrupedal
posture or locomotion in Australopithecus. In partic-
ular, the valgus angle of the knee of hominids is an
epigenetically labile trait (Tardieu and Trinkaus,
1994; Duren and Ward, 1995; Duren, 1999) and
demonstrates that A. afarensis walked upright not
quadrupedally. In a recent study of the development
of a valgus knee in humans in normal and nonam-
bulatory myelodysplastic children, Duren (1999)
found that a bicondylar angle was the direct result of
a habitual bipedal gait. It does not form in these
affected individuals who engage only in intermit-
tent, or facultative, bipedality. The presence of a
valgus knee in Australopithecus demonstrates that
it was a habitual biped, falsifying the hypothesis of
Sarmiento (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 repertoire
in these taxa. Alternately, they could be homopla-
sies evolved for different purposes in hominins and
gorillas. Therefore, this hypothesis will not be dealt
with further here.
187
The second hypothesis is the first of two that have
received much broader support by data and by the
paleoanthropological community. This position has
been articulated most clearly and extensively by
Stern, Susman, and Jungers (summarized by Stern,
2000), and states that A. afarensis individuals were
primarily terrestrial bipeds, but they also climbed
trees (e.g., Senut, 1980; Berge and Ponge, 1983;
Jungers and Stern, 1983; Schmid, 1983; Stern and
Susman, 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 the
mosaic of morphological features found in the A.
afarensis skeleton (see McHenry, 1994; Stern, 2000).
They acknowledged the suite of features reflecting
upright bipedal progression, but also emphasized
numerous ape-like characters. They argued that
when reconstructing the probable positional behav-
iors of A. afarensis, as for any fossil taxon, one must
consider the total morphological pattern evident in a
skeleton (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 any
primitive traits retained in the skeleton, they must
be there for a functional reason. Some researchers
have gone one step further, suggesting that A. afa-
rensis exhibits a compromise morphology, and that
these primitive traits would have affected the na-
ture of bipedal progression in Australopithecus
(Stern and Susman, 1983; Jungers, 1982; Jungers
and 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 widespread
support. The most widely published proponents of
this idea are Latimer, Lovejoy, and Ohman, and the
clearest articulation of their perspective can be
found 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 because
A. afarensis had not only acquired adaptations for
bipedality, it had, in the process, reduced its arbo-
real efficiency by sacrificing traits such as relatively
long forelimbs, fingers, and toes, and perhaps most
importantly, a grasping foot (Latimer and Lovejoy,
1989; Latimer, 1991). They cite the clear vector of
morphological change (defined as the magnitude
and direction of morphological character transfor-
mation throughout a lineage; Simpson, 1953) that
was towards anatomy that enhanced terrestrial
bipedality and diminished arboreal competence
(Latimer, 1991). Thus, the shift away from features
enhancing 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 for
survival and reproduction in A. afarensis and its
immediate ancestors. They argue that if A. afarensis
188 YEARBOOK OF PHYSICAL ANTHROPOLOGY
individuals did climb trees, arboreal agility had lit-
tle adaptive significance for them. Although at one
point Lovejoy (1988) went one step further to add
that A. afarensis not only was not adapted to climb
trees, but could not have done so effectively without
adverse consequences for their fitness, he later re-
turned to the argument that that it simply is not
possible to determine the fitness benefits of arbore-
ality in A. afarensis (Ohman et al., 1997).
In summary, these latter two hypotheses about
early hominin locomotion are in complete accord
over the fact that the recent ancestors of A. afarensis
had 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 nature
of early hominin bipedality is to understand the
nature of the disagreements over interpretations of
A. afarensis locomotion. The debate is not due to a
lack of fossil evidence, because A. afarensis is known
from most skeletal elements. There are a few dis-
agreements over interpretations of available fossil
evidence (summarized in Stern, 2000), but the de-
bate has two more significant causes. First, re-
searchers have different approaches to interpreting
anatomy, and in particular primitive retentions
(Latimer, 1991; Coffing, 1999). Second, and equally
importantly, they are asking fundamentally differ-
ent questions of the data.
One reason for the disagreement over Australo-
pithecus locomotion is a fundamental philosophical
difference in the interpretation of primitive charac-
ters (Coffing, 1999). Derived signals in morphology
are relatively easy to interpret. The numerous de-
rived traits of Australopithecus have been shown by
biomechanical analyses to be accommodations for
weight-bearing and movement in upright bipedal
posture. These features, like sinusoidal vertebral
curvatures or an adducted hallux, are unambiguous,
and are considered adaptations to habitual upright
posture and locomotion. Their unambiguous polar-
ity, coupled with their clear affect on function (in the
sense of Lauder, 1996: the use or action of pheno-
typic features), reveals their biological role (again as
in Lauder, 1996: the role of phenotypic features in a
specific environmental or ecological setting) for bi-
pedal progression (Weishampel, 1995). These char-
acters tell us that the ability to walk upright
conferred significant fitness benefits on those indi-
viduals better designed to deal with the mechanical
demands of terrestrial bipedality.
The ape-like features of Australopithecus, on the
other hand, are generally assumed to be primitive
retentions (lists in McHenry, 1994; Stern, 2000), and
many probably are. Interpreting why these primi-
tive features are retained in A. afarensis, or any
taxon, is where perspectives diverge. Australopithe-
cus had undergone numerous modifications that
served to enhance terrestrial bipedal function at the
[Vol. 45, 2002
expense of arboreal function, most notably the loss
of a divergent hallux, reduction in intermembral
index, and shorter fingers and toes. These changes
imply that agile movement in the trees was of lesser
reproductive 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 arboreal
competence did not result in a selective disadvan-
tage to the immediate ancestors of A. afarensis,
however.
In this case, the retention of features ordinarily
associated with arboreal progression, such as fore-
limbs longer relative to hindlimbs, or phalanges
longer and more curved compared with those of hu-
mans, is inherently difficult to explain (see Gould
and Lewontin, 1979; Bock, 1980, Baum and Larson,
1991; VanValkenburgh, 1994; Lauder, 1995, 1996).
Such traits could have been actively retained by
stabilizing selection because they continued to en-
hance the survival and reproductive success of their
bearers by enabling them to be more agile tree
climbers 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 may
even have been in the process of being selected
against (disaptations; Gould and Vrba, 1982). Be-
cause any of these three mechanisms can occur, and
undoubtedly does occur, these hypotheses are im-
possible to test without further information.
Latimer, Lovejoy, and Ohman argue that because
we cannot readily test these hypotheses, we cannot
consider the adaptive value of retained primitive
traits. Stern, Susman, and Jungers, on the other
hand, argue that the stabilizing selection hypothesis
is the only logical one to explain the maintenance of
the numerous primitive features of A. afarensis. Bi-
ases towards one hypothesis can color researchers’
interpretations of the adaptive role of morphological
structures, and thus the biology and behavior of
extinct animals.
The second, and equally important, reason for the
disagreement over Australopithecus locomotion is
that these two sets of researchers are asking differ-
ent questions. Latimer, Lovejoy, and Ohman are
interested in attempting to reconstruct the pattern
of natural selection that produced A. afarensis: why
did A. afarensis evolve? They would argue that it
does not matter what actual activities individuals
engaged in over the course of the day; the strength of
selection on a particular trait that affects a behavior
is not proportional to the time the individual en-
gages in that behavior. Individuals sit, sleep, and
engage in many other activities that do not impose
adaptively significant consequences on those indi-
viduals that do not possess morphologies particu-
larly suited to those activities. In other words, all
activities do not have the same fitness effects with
respect to the skeleton. They argue that we simply
Ward] INTERPRETING A. AFARENSIS LOCOMOTION
cannot know, nor is it necessary to know, all of the
behaviors in which the animals engaged. If we are
interested in reconstructing adaptive history, then it
is the vectors of morphological change (Simpson,
1953) that will reflect vectors of selection acting on a
lineage, and provide the answers we seek (Latimer,
1991). Stabilizing selection is harder to discriminate
from lack of selection for primitive structures,
Latimer (1991) argues, so we must restrict basing
our hypotheses about selective pressures that
shaped a lineage to evidence from directional change
within 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 infer
the actual behavioral repertoires of A. afarensis in-
dividuals, and not the history of selection. These
researchers note that individuals engage in varied
locomotor activities over the course of days and life-
times. Their approach seeks to identify what types of
behaviors one might see A. afarensis engaged in if
one traveled back in time to observe them: what was
their locomotor repertoire? Stern (2000) chooses a
quote from Duncan et al. (1994, p. 79) that summa-
rizes their philosophy: “understanding the overall
functional pattern (emphasis mine) of the organism
requires an equal consideration of all its anatomical
features, 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 Jungers
argue that this approach is indeed important, be-
cause in order to understand our ancestors, we need
to be able to reconstruct their behavior.
These two approaches are different, and comple-
mentary rather than mutually exclusive. Thus, the
apparent debate as it has been framed is not a true
debate. It is important to keep in mind the distinc-
tion between reconstructing behaviors from recon-
structing evolutionary pressures. Neither approach
to understanding Australopithecus is better or worse
than the other. They are intrinsically different, how-
ever. They address the data differently, and rely on
different characters for different reasons. They
should not be contrasted as opposite sides of a single
argument. Both questions are worth pursuing. We
need to understand the types of animals early homi-
nins were, as well as the history of selection that
shaped them. It is time to recognize the differences
in 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 our
approach to interpreting the fossils. The first step is
to be explicit about what questions we are asking.
Do we want to reconstruct the history of natural
selection shaping the hominin lineage(s), or the lo-
comotor/behavioral repertoires of fossil taxa? The
189
next step is to identify specific hypotheses and cri-
teria for their potential falsification. To address the
question of selective history, we first must under-
stand the polarity of traits we are considering, and
the vectors of morphological change apparent in the
early hominin skeleton. To answer either question,
we need to better understand morphology and its
influences. Not all traits provide similar information
about fossil taxa (e.g., Cartmill, 1994; Churchill,
1996; Lieberman, 1997; Lovejoy et al., 1999, 2000).
Some will tell us more about genetic change within
a species, and therefore the history of selection, and
some will tell us more about an individual’s behavior
over the course of its lifetime.
Hypotheses about adaptation
To infer the selective regime acting on a species
from morphology alone is notoriously difficult, and a
substantial literature is devoted to this issue (e.g.,
Gans, 1966; Gould and Lewontin, 1979; Bock, 1980;
Wake, 1982; Arnold, 1983; Mayr, 1983; Baum and
Larson, 1991; Leroi et al., 1994; Koehl, 1996; papers
and references in Thomason, 1995; Rose and
Lauder, 1996). Without ecological data and data
about which behaviors affect fitness in which ways,
we lack critical information that would enable us to
actually test hypotheses about the selective regimes
acting on A. afarensis (Baum and Larson, 1991;
Koehl, 1996; Larson and Losos, 1996). Instead, we
must rely on phylogeny, biomechanical modeling,
and comparative morphology to support or refute
hypotheses about selective pressures as best we can.
To construct hypotheses about the selective re-
gime that shaped a taxon, one must first identify the
character 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 about
extant hominoid relationships (see Ruvolo, 1997).
This may not be enough to reconstruct the character
states of the last common ancestor of apes and homi-
nins, however. The burgeoning fossil record of Mio-
cene and Pliocene apes, including hominins, slowly
continues to add more data with which to develop
and test phylogenetic hypotheses among living and
fossil taxa. Because these fossil taxa do not resemble
extant species in all features, they stand to alter the
balance of parsimony for traits, and so could affect
our interpretations of the primitive conditions from
which Australopithecus or other early hominins
evolved. Continual attention to phylogenetic analy-
ses of hominoids will be critical to our ability to
reconstruct character transformations that pro-
duced Australopithecus and other early hominins.
While drift and other random forces may have
lasting impacts on species over time (see Nitecki,
190 YEARBOOK OF PHYSICAL ANTHROPOLOGY
1990), the only evolutionary force that can produce
long-term directional change is selection, particu-
larly when there is a broad suite of features that all
enhance the same function, e.g., bipedality in Aus-
tralopithecus. Therefore, it is reasonable to infer
that when long-term directional change is observed
within a lineage, especially in numerous characters
or character complexes, that selection for a behavior
influenced by the observed morphology was the
cause.
Biomechanical modeling and comparative studies
can help reveal the biological roles of the newly
transformed 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 hypotheses
about the behaviors on which selection acted. If phy-
logenetic analysis determines that a structure is
apomorphic, and mechanical analysis determines
the function it enhances, we can hypothesize that
selection for that function produced the structure
(Weishampel. 1995). Comparative morphological
and behavioral studies can be used to support hy-
potheses of adaptation when similarly constructed
modern animals are known to share a similar func-
tion. In the case of A. afarensis, there are numerous
derived modifications of their skeletons that en-
hance terrestrial bipedal progression and resemble
modern hominoid bipeds. Thus, we can hypothesize
that these characters were shaped by selection for
bipedal locomotor abilities.
Testing hypotheses about the retention of primi-
tive traits is more difficult (e.g., Frumhoff and
Reeve, 1994). When a primitive trait remains un-
modified in a taxon from the ancestral form, the null
hypothesis is that it is selectively neutral, termed a
secondary nonaptation (Lauder, 1996). To falsify the
null hypothesis, one must be able to show that sta-
bilizing selection or negative selection was at work.
To demonstrate stabilizing selection for a primitive
trait, one would need to show that the primitive
structure compromised a derived function. In the
case of Australopithecus, this would be whether its
primitive traits compromised bipedality.
Other lines of evidence might be invoked as
weaker support for the hypothesis of stabilizing se-
lection. If a trait was retained in its unmodified form
for a substantial period of time (stasis), it is possible,
but not certain, that stabilizing selection was in-
volved. If one could demonstrate that an animal
actually engaged in behaviors for which the primi-
tive traits had been adaptations, it might suggest
continued adaptive value of these traits, but again
this would not be definitive. Even if these latter two
criteria (stasis or behavior) were met, they would
still not falsify the null hypothesis of nonaptation.
They merely would be suggestive. If a trait was
selectively neutral, variation should increase over
time (e.g., Tague, 1997, 2002a). However, the lack of
increased variability still might not signal stabiliz-
[Vol. 45, 2002
ing selection. Even if a trait was neutral with re-
spect to selection, a trait could be pleiotropically or
structurally linked to other traits that were under
selective influence. Its maintenance could reflect
lack of selection to change a developmental cascade
influencing other structures that are themselves be-
ing maintained by stabilizing selection (discussions
in Maynard Smith et al., 1985; Churchill, 1996).
A final hypothesis for the retention of primitive
traits could be that they were actively being selected
against, but that selection had not had sufficient
time to reduce or eliminate them. This hypothesis of
disaptation 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 in
A. afarensis lies in the interpretation of the rudi-
mentary forelimbs in Tyrannosaurus rex (Carpenter
and 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 directional
signal towards a new behavior, terrestrial bipedal-
ity. So, are these tiny forelimbs still present because
they serve an adaptive function for some altered
task, or are they retained for no reason? Some of the
debate over their function takes the form of logical
arguments, which are not necessarily empirical (Os-
born, 1906; Newman, 1970; Paul, 1988). The most
recent contribution uses forelimb bone robusticity
and inferred muscle size and strength to argue that
these are not useless, vestigial structures (Carpen-
ter and Smith, 2001). Because both of these features
are influenced by behavior, this evidence suggests
that the forelimbs were still used for some purpose,
which Carpenter and Smith (2001) hypothesize was
manipulating 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 their
original function. It is, however, a useful example to
explore 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 the
question was if the structure was functional at all or
merely vestigial, a more relevant example is the
hindlimbs of the primitive whale Ambulocetus
(Thewissen et al., 1994). The retention of functional
hindlimbs in this taxon indicates that it could am-
bulate terrestrially, although there was a clear di-
rectional signal towards an aquatic lifestyle. The
authors propose that the hindlimbs were propulsive
in the water and on the land. The vector of morpho-
logical change clearly was towards improving swim-
ming ability at the expense of terrestriality. When
Ambulocetus was terrestrial, it would have been rel-
atively awkward in its movements. Knowing that it
could have moved about on land, and even that it
may have done so, it is still difficult to assess the
adaptive significance of terrestriality in these early
whales. Again, here the fossil record reveals the
Ward] INTERPRETING A. AFARENSIS LOCOMOTION 191

Fig. 1. Molar shearing quotients in extant and early Miocene hominoids. Early Miocene apes have lower crests, but microwear
analyses demonstrate that they had a similar range of diets to extant taxa. This illustrates a disjunction between behavior and
anatomy 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).

vector of morphological change, but reconstructing
the pattern of selection that produced this change
relies 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 necessarily
different. The retention of primitive traits does not
always mean that these traits were maintained for
their original function. Examples of discrepancies in
form-function relationships between extant and fos-
sil taxa can and have been demonstrated between
tooth morphology and diet, for which evidence of
genetically based morphology (tooth form) can be
compared to evidence of behavior (microwear and
bone isotope analysis). One example of this phenom-
enon was found in the teeth of late Miocene/early
Pliocene horses from Florida (MacFadden et al.,
1999). All six species examined in this study re-
tained inherited high-crowned molars, and based on
tooth morphology would have been interpreted as
grazers of abrasive C4 grasses. However, microwear
and isotope data suggest that they had a range of
diets from browsing to grazing on many types of C3
and C4 plants. Some species (particularly Dinohip-
pus mexicanus and Astrohippus stockii) were almost
exclusively browsers. Hypsodonty appears to have
been retained, perhaps because of some sort of phy-
logenetic and/or developmental constraint, although
behavior had changed.
Another example comes from the primate litera-
ture. Kay and Ungar (1997) showed that although
Miocene apes had a similar range of molar shearing
crest lengths as do roughly the same taxonomic di-
versity of extant species, the molars of all early
Miocene taxa were all more bunodont than those of
extant apes (Fig. 1). These data seem to suggest that
no Miocene apes were as folivorous as the most
folivorous extant apes, i.e., gorillas and siamangs.
This may be incorrect, as Kay and Ungar (1997)
argued using microwear data. Their microwear
192 YEARBOOK OF PHYSICAL ANTHROPOLOGY
analyses showed that, in fact, the Miocene taxa were
eating the same range of diets seen in extant apes,
and that even species such as Rangwapithecus,
which had teeth with gross morphology most like
those of modern frugivores, were eating as many
leaves as do modern folivores. In effect, tooth mor-
phology improved over time.
This may well have happened in the evolution of
hominin, and hominoid, postcranial anatomy, and it
may be possible to uncover the extent to which it
may have occurred by comparing traits with greater
or 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 resolution
possible in the fossil record. For example, humans in
many forager groups like the Yanamamo (Chagnon,
1997) and Achuar climb trees for fruit and other food
resources (Descola, 1996a,b). This behavior is not
reflected in genetically determined skeletal mor-
phology, because anatomical variation that im-
proves arboreal abilities apparently has not affected
their fitness. We would not be able to “see” the
arboreality in their skeletons, just as we cannot
“see” behaviors such as lying down or sitting, be-
cause an individual’s anatomy does not affect his
fitness by allowing him to be more or less effective at
these behaviors (Latimer, 1991). There is no selec-
tive disadvantage of having anatomy that is poorly
designed for such tasks. This makes interpreting
actual behaviors in extinct species particularly
tricky. It may be possible at some level, but will
always remain unsatisfying at another. If A. afaren-
sis climbed trees, we have to be clever enough to find
ways to read this in their morphology, potentially
using ontogenetically labile characters that can be
influenced by individual behaviors over the course of
a lifetime. Still, it is worth the attempt, so that we
can better understand what our extinct relatives
were like.
The simple presence of primitive features in the A.
afarensis skeleton is not enough to identify the
adaptive value of tree climbing. For example, a fu-
ture paleoanthropologist studying skeletons of to-
day’s humans could argue that because we retained
a grasping hand and mobile shoulder joint, features
that evolved for an arboreal lifestyle, modern hu-
mans are partly arboreal. None of us, however,
would argue that these traits were maintained by
selection on humans primarily for the ability to
climb trees well. Instead, these traits primarily rep-
resent exaptations for manipulative or throwing
abilities, although they also are used in climbing
rocks or trees.
Behavior of an extinct animal can be examined by
considering morphological features that are shaped
by its activity pattern. One of the best examples of
an environmentally determined trait is dental mi-
[Vol. 45, 2002
crowear, the pits and scratches on teeth caused by
diet. Given a constant pattern of enamel microstruc-
ture and fracture behavior, which appears to be the
case for all hominoids, microwear reveals individual
activity, but not adaptive history (Teaford, 1988,
1994). In contrast, because tooth shape appears to
be conservative within taxa, it is generally assumed
to be tightly genetically controlled, and not influ-
enced by an individual’s diet (although fetal envi-
ronment and nutrition may be involved in tooth
formation, 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 and
Hiiemae, 1974; Kay, 1975; Rosenberger and Kinzey,
1976; Strait, 1993a, b; Teaford, 2000). Tooth shape
and features such as molar shearing crest length
reflect a history of selection, whereas microwear re-
flects behavior.
Unfortunately, postcranial anatomy has few, if
any, such dichotomies. Examples of epigenetically
plastic traits are physeal plate angles (Tardieu and
Trinkaus, 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 of
joint conformation (Frost, 1979, 1994; Hamrick,
1999; but see Lieberman and Pearson, 2001). By
carefully studying the influences of activity on bone
form, either directly or via soft tissues, we will be
better able to use morphological information reliably
to reconstruct behavior. By identifying the develop-
mental plasticity of morphology, we are better
armed to reconstruct the behavioral repertoires of
fossils, and to avoid misinterpreting characters
when constructing phylogenies with morphological
data.
REEXAMINATION OF THE FOSSIL EVIDENCE
USING THIS FRAMEWORK
Armed with a more explicit identification of the
questions we are asking about Australopithecus, we
can begin to reevaluate the fossil record for early
hominin locomotion using this empirical framework.
For all phases of this process, it is important to
elucidate the genetic and ontogenetic influences on
morphology.
Character polarities and vectors of
morphological change in early hominins
Reconstructing character transformations within
hominoid lineages is notoriously difficult (Larson,
1998; Sarmiento, 1998; Begun, 1999; Richmond et
al., 2001). Despite studies arguing that postcranial
data are more informative about phylogeny than are
craniodental data (Collard and Wood, 2000), it is not
the case that we can assume hominins evolved from
an ancestor that was similar to extant great apes in
Ward] INTERPRETING A. AFARENSIS LOCOMOTION
every aspect of its postcranial anatomy. Recent at-
tention to the amount of apparent homoplasy in the
hominin skeleton (e.g., Larson, 1996, 1988; Begun et
al., 1997a, b; Rose, 1997; Ward CV, 1997; Lieber-
man, 1999; Coffing and McHenry, 2000; Collard and
Wood, 2000; MacLatchy et al., 2000) highlights our
need to remain cautious in making polarity deter-
minations, especially based on extant hominoid data
alone. Elucidating the genetic and ontogenetic influ-
ences on morphology will aid in the understanding
of 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 most
effective only by including all available data in con-
structing the phylogenies upon which we base our
polarity determinations.
Character selection determines our ability to
make accurate phylogenetic hypotheses. This re-
quires careful choices of features, and knowledge
about the individual variability, phenotypic plastic-
ity, and heritability of traits (e.g., Cartmill, 1994;
Weishampel, 1995; Lieberman, 1997, 1999), as well
about genetic and ontogenetic links among them. As
the determinants of adult form become clearer, and
we can identify behavioral or functional influences
on morphology, we can use these inferences to make
hypotheses about the behaviors of A. afarensis and
its ancestors, allowing us to reconstruct the history
of selection that led to bipedality (Richmond and
Strait, 2000; Richmond et al., 2001 and references
therein). Functional anatomy is not unrelated to
phylogenetic reconstruction, as it both informs char-
acter selection and provides a venue in which to test
phylogenetic hypotheses (Brooks and MacLennan,
1991; Harvey and Pagel, 1991; Weishampel, 1995;
Witmer, 1995; Begun et al., 1997a; Ward et al.,
1997). Functional and phylogenetic interpretations
are codependent. Thus, our phylogenetic reconstruc-
tions are critical to reconstructing the vectors of
change.
Based on extant hominoid taxa alone, our percep-
tion of character transformation would be relatively
straightforward. All four great ape species share a
suite of morphologies that enhance their abilities to
engage in vertical climbing and below-branch arbo-
real activities, given their relatively large body
sizes. These include a strongly grasping hallux and
pollex, a restructured torso involving laterally facing
shoulder joints, a high intermembral index, long,
curved phalanges, strong manual and pedal grasps,
short lumbar vertebral columns, and craniocaudally
elongate pelves. Modern great apes differ in compar-
atively minor ways. With no further information,
it would seem clear that these shared features
were indisputably homologous, and that hominins
evolved from an ancestor that was postcranially
much 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-
193
ing them to reconstruct character transformation
through hominoids can we come close to uncovering
actual patterns of change in hominoid evolution. By
incorporating 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 fossil
apes is problematic, of course. Furthermore, we can
never hope to recover the diversity of hominoid species
that must have existed. Nonetheless, without consid-
ering what we do know and making careful hypotheses
about the relationships we have identified so far, we
neglect vital information about the pattern of evolu-
tionary history that produced living hominoids. This
information may alter our perceptions of which homi-
nin features are, in fact, derived, and which are prim-
itive.
A recently published phylogeny of hominoids
based on 240 characters of craniofacial, dental, and
postcranial skeletons is the most robust phylogeny
of these taxa constructed to date (Fig. 2) (Begun et
al., 1997a). Using this as a baseline, we can examine
the 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 and
among pedal digits, or overall foot length. Still, the
approach 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 in
the realization that extant great apes’ postcranial
anatomy may not all be homologous. Sivapithecus is
widely considered to be the sister taxon of Pongo
(review in Ward S, 1997). Because humeral torsion
is 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 of
torso 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 behavior
pattern; 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, instead
more 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 extant
orangutans or African apes, and shorter, less curved
2
Moyà-Solà and Köhler (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.
194 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 45, 2002

Fig. 2. Phylogenetic hypothesis of living and fossil hominoid relationships modified from Begun et al. (1997b). Diagram is a
consensus tree based on 240 cranial and postcranial characters, and so is the most comprehensiveanalysis of these materials published
to 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 considered
separately.

phalanges (Rose, 1986, 1997; Spoor et al., 1991;
Begun, 1993). Their inferred torso structure, which
reflects a ventrally oriented scapular glenoid fossae
and an emphasis on flexion-extension abilities of the
proximal forelimb at the expense of abduction-ad-
duction movements, and appendicular characters
perhaps indicating less well-developed manual and
pedal grasping ability, are more like those of basal
hominoids such as Proconsul (summarized in Ward
S, 1997).
These Sivapithecus postcranial fossils imply that
either Pongo is convergent upon African apes in
many of its more specialized climbing features, or
that the many craniofacial similarities of Pongo and
Sivapithecus are homoplasies (Pilbeam et al., 1990;
Ward S, 1997). Either of these hypotheses is plausi-
ble, but they are mutually exclusive. The possibility
of Asian and African great apes sharing postcranial
homoplasies linked with below-branch arboreality is
not unreasonable, given the apparent independent
acquisition 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 in
closely related organisms subjected to similar selec-
tive pressures (e.g., Jolly, 2001). The likelihood of
independent acquisition of the Pongo and Sivapithe-
cus craniofacial similarities is less certain at this
point (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/or
Equatorius, and with Hylobates, that are not found
among extant great apes, such as shorter pelves
with longer lumbar vertebral columns, less curved
forelimb bones, longer thumbs, shorter medial rays
of 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 known
from the fossil record after Proconsul, whose feet
were not as long as those of extant apes (Walker and
Teaford, 1988). Either hominins have reverted to the
primitive condition in these features, or extant apes
are homoplastic in these ways. Either scenario in-
volves substantial homoplasy, making polarity de-
terminations among hominoids difficult.
Ward] INTERPRETING A. AFARENSIS LOCOMOTION
The likely Asian-African ape homoplasies open
the possibility that chimps and gorillas may also be
homoplastic in some features. This hypothesis is
supported by some researchers studying kinematic
and anatomical correlates of knuckle-walking in
chimps and gorillas (Inouye, 1994; Dainton and Ma-
cho, 1999). If so, some of these hominin characters
may be primitive, which would indicate less change
from the last common ancestor than we now sup-
pose. Recently, however, strong arguments were
made 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 the
most widely accepted at present. Further research
into the function and evolution of the forelimb is
needed 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 even
when the fossil evidence is considered. A long pisi-
form, dorsoplantarly narrow navicular, and meta-
tarsals lacking expanded dorsal margins of their
head are known for Oreopithecus (Sarmiento, 1987)
and extant apes. Australopithecus lacks the ex-
panded vertebral bodies of humans, resembling all
taxa for which there are data (e.g., McHenry, 1992):
Proconsul (Napier and Davis, 1959; Walker and
Pickford, 1983; Walker and Teaford, 1988; Ward et
al., 1993), Nacholapithecus (Rose et al., 1996a,b;
Nakatsukasa et al., 1998, 2000), Equatorius (Le
Gros Clark and Leakey, 1951), Morotopithecus
(Walker and Rose, 1968; Gebo et al., 1997; Mac-
Latchy et al., 2000), Oreopithecus (Harrison, 1986;
Sarmiento, 1987), Dryopithecus (Moyà-Solà and
Köhler, 1996), and extant primates. Within the
hand, a pronounced third metacarpal styloid pro-
cess, found only in Homo and some gorillas, is ab-
sent in Proconsul (Napier and Davis, 1959) and
Oreopithecus (Moyà-Solà et al., 1999). Also, the first
metacarpal base highly is concavoconvex in Procon-
sul (personal observation), Sivapithecus (Spoor et
al., 1991), Oreopithecus (Moyà-Solà et al., 1999), and
extant apes. Small apical tufts are found on the
distal phalanges of Afropithecus (Leakey et al.,
1988), Proconsul (Napier and Davis, 1959; Begun,
1994), Nacholapithecus (Nakatsukasa et al., 1998),
Oreopithecus (Moyà-Solà et al., 1999), Dryopithecus
(Moyà-Solà and Köhler, 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 flexor
ridges are found in Oreopithecus (Harrison, 1986;
Sarmiento, 1987; Moyà-Solà et al., 1999), Dryopithe-
cus (Begun, 1992, 1993; Moyà-Solà and Köhler,
195
1996), Orrorin (Senut et al., 2001), and Ardipithecus
(Haile-Selassie, 2001), and in extant apes, although
less 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 hamulus
appears 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). Hamulus
form likely reflects morphology of the carpal tunnel
rather than flexor carpi ulnaris function, as previ-
ously suggested (Sarmiento, 1998; Ward et al.,
1999b). However, the pisohamate ligament inserts
not 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 or
pisohamate ligament, but the palmar carpal liga-
ment (flexor retinaculum), which forms the roof of
the carpal tunnel. It is certainly possible that carpal
tunnel length is related to overall hand length, and
if so, hamulus distal projection may be related to
hand length at least at some level. A. afarensis ap-
pears to have reduced the proximodistal length of its
carpal tunnel relative to African apes.
The high intermembral index (calculated as (hu-
merus ⫹ radius/femur ⫹ tibia) * 100) of African apes
appears to have been present in at least Oreopithe-
cus (Hürzeler, 1960; Moyà-Solà and Köhler, 1996)
and Dryopithecus (Moyà-Solà and Köhler, 1996), al-
though not in Proconsul (Walker and Pickford, 1983;
Walker and Teaford, 1988). Although Dryopithecus
was interpreted to have an intermembral index
higher than that of African apes and only like oran-
gutans among extant species (Moyà-Solà and
Köhler, 1996), it may not have been as extreme, as
these data were based on extensive segment length
reconstructions. Direct comparison of the reported
ulna to femur lengths published with the fossil an-
nouncement (Moyà-Solà and Köhler, 1996) is 102,
close to the African ape range (chimpanzees, 87–97;
gorillas, 91–101), and considerably less than that of
orangutans (128 –130). Oreopithecus, on the other
hand, is intermediate between extant African and
Asian apes, with an ulna/femur ratio of 111. Austra-
lopithecus had an ulna (length estimate based on
Drapeau, 2001) to femur length of about 80, showing
an apparent reduction in forelimb to hindlimb pro-
portions. This is evident in comparisons of humeral
to femoral proportions as well (Jungers, 1982, 1994;
Wolpoff, 1983; White et al., 1993; White, 1994).
3
In this paper, the term Homo is used to include Homo erectus/
ergaster and more recent members of the genus Homo only, following
the grade-based approach of Wood and Collard (1999).
196 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 45, 2002
Within the forelimb, A. afarensis also appears to
be 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, and
Oreopithecus, she demonstrated that the slightly
higher brachial index of Australopithecus compared
with extant apes (see Kimbel et al., 1994) appears to
represent 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 than
often assumed (Jungers, 1982, 1994; Wolpoff, 1983;
White et al., 1993; White, 1994). There is thus no
evidence that A. afarensis is derived in forelimb
proportions, supporting the hypothesis that their
lower limbs are elongated rather than their fore-
limbs reduced (Wolpoff, 1983). Instead, Pan and
Pongo, and to a lesser extent Gorilla, seem to have
independently elongated their forearms from the
likely ancestral condition.
Another important finding by Drapeau (2001) is
that chimpanzees and bonobos have uniquely long
metacarpals relative to their forearm lengths among
extant and fossil hominoids. Australopithecus meta- Fig. 3. Proximal femurs and tibias of Homo sapiens, Austra-
lopithecus afarensis AL 288-1, and Pan troglodytes. Note similar
carpals are the same length relative to the forearms location of presumed muscle attachments in A. afarensis and in
as in all extant hominoids except Pan. This discov- chimpanzee. Line drawings modified from Aiello and Dean
ery highlights the potential error in assuming that (1990).
Pan reflects the morphology of the last common
ancestor.
A number of primitive characters of A. afarensis afarensis, however, these muscles had an extant
appear to reflect soft-tissue differences from hu- ape-like conformation, with a discrete bony insertion
mans, and suggest a somewhat more extant great along the medial margin of the tibial tuberosity,
ape-like muscular configuration in these early homi- leaving a roughened pit in the bone (Fig. 3). Al-
nins. Some of the Australopithecus hip and thigh though there is no bony evidence of it, on the lateral
muscle attachment sites appear to have differed side of the knee in chimpanzees and gorillas, the
from those of Homo. Instead, they more closely re- biceps femoris extends to the lateral side of the tibial
semble those of extant apes, and as best as can be tuberosity but blends with the crural fascia, with no
determined, fossil taxa as well. First, there is a evident bony insertion (personal observation). It is
large, roughened ovoid area on the anterolateral at least possible that this would have been the case
border of the greater trochanter (Fig. 3), which ap- in Australopithecus, given the ape-like medial side
pears to have been for attachment of the anterior of the knee. The conformation of the A. afarensis
fibers of gluteus minimus, which on great apes is ischial tuberosity also differs from that of humans,
sometimes a separate muscle called the scansorius. being longer, with the adductor magnus origin site
In humans, this muscle attaches on the anterosupe- set at an angle to the rest of the tuberosity. This
rior portion of the trochanter, and does not extend different conformation may reflect other primitive
distally. Häusler (2001) reconstructs the gluteal musculature.
muscles of A. afarensis and A. africanus as essen- Latimer and Lovejoy (1990b) suggest that the con-
tially human-like, although with a slightly ex- vex first metatarsal head of A. afarensis, unlike the
panded anterior portion of the gluteus medius (con- flatter configuration in humans, may reflect more
tra Berge, 1994). These observations are consistent idiosyncratic loading in A. afaernsis than in Homo.
with the hypothesis of Robinson (1972) that the They argue this may be due to the fact that the
large anterior lesser gluteals could compensate by triceps surae may not yet have undergone the
the slightly less sagittal orientation of the iliac changes in muscle belly length and pennation seen
blades. in humans, and so relatively more plantarflexion
The medial thigh muscles of A. afarensis also ap- was accomplished with the peroneal muscles. The
pear to have differed in their distal insertions. In large peroneal muscles are suggested by the large
humans, the sartorius, gracilis, and semitendinosus peroneal groove on the fibula and peroneal trochlea
have a common fan-shaped insertion called the pes on the calcaneus (Latimer and Lovejoy, 1989,
ansirinus that largely blends with the crural fascia 1990b). This hypothesis is difficult to test, as mus-
along the medial side of the proximal tibia. In A. cles do not fossilize. Given the lack of capacity for
Ward] INTERPRETING A. AFARENSIS LOCOMOTION
hallucal abduction in any Australopithecus, it is
highly unlikely that the rounded head of the first
metatarsal reflects opposability, but whether it
somehow reflects arboreality is unspecified and un-
known.
Taken together, though, these indicators of a
somewhat primitive muscle configuration in Austra-
lopithecus suggest that these early hominins were
not fully modern in their muscular anatomy. This is
an important point, because when muscles contract
to respond to ground reaction forces or produce
movement, they generate strain within bones that
can trigger modeling responses during growth and
remodeling after skeletal maturity (review and dis-
cussion in Martin et al., 1998; Carter and Beaupré,
2001). This means that some bony differences be-
tween Australopithecus and humans could be re-
lated to one of two factors, or both. Either these
hominins were behaving differently, or they were
behaving in the same way but with slightly different
muscle vectors due to the primitive muscle arrange-
ment. The latter situation could produce a slightly
different pattern of bone strain, influencing traits
such as the geometry of the acetabulum, proximal
femoral shaft, patellar groove, or hallucal tarso-
metatarsal joint shape. Indeed, Berge (1991) hy-
pothesized that A. afarensis only could have moved
bipedally efficiently if it had a more ape-like ar-
rangement of the hip musculature due to its slightly
different bone structure. Although these ideas have
not been tested, they represent a plausible alternate
hypothesis that should be considered when evaluat-
ing skeletal differences among hominins.
Another feature in which A. afarensis has been
considered significantly different from humans is in
the anteroposteriorly compressed sacral ala. How-
ever, given the mediolaterally extensive and antero-
posteriorly compressed nature of the A. afarensis
pelvis, and the broadly flaring blades, this feature
may 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 available
for the earliest putative hominins Sahelanthropus,
Orrorin, and Ardipithecus. All three genera have
been described as probable bipeds, but the nature of
this bipedality and their morphological similarity to
later hominins are still unknown or undescribed.
Sahelanthropus is known only from a cranium. Be-
cause it has a short basicranium with the basion
intersected 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 they
mention in their article, however, are exclusively
found in bipeds. It could be that when the internal
contours of the femoral neck are revealed, and when
proximal to middle shaft dimensions are compared,
the data will be sufficient to make a judgment. Ar-
197
dipithecus has also been described as a biped, based
on a short basicranium in A. ramidus ramidus
(White et al., 1994) as in Sahelanthropus (Brunet et
al., 2002), and on a proximal phalanx of A. ramidus
kedabba that resembles those at Hadar (Haile-
Selassie, 2001). A. r. kedabba also appears to have
had a curved ulna, but this is found in hominin
ulnas from the Omo River Valley (Omo L40-19) and
Olduvai 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 have
been published so far.
So, in summary, most features of A. afarensis that
are generally interpreted to be primitive probably
are, although the prevalence of homoplasy among
hominoids should suggest caution in making this
assumption. The likely homoplasies between Asian
and African apes raise the possibility that African
apes may be convergent upon one another in ways
other than forelimb length, making some apparently
derived hominin features possible homoplasies, such
as relatively short forelimbs, short pelves, 5– 6 lum-
bar vertebrae, and thumb-finger proportions. This
could be true even if the last common ancestor of
African apes and humans was a knuckle-walker.
Some features that appeared to be derived in A.
afarensis, such as the short metacarpals or forelimb
proportions, appear to be primitive, with extant apes
often displaying a derived condition. Extant apes
cannot be assumed to represent the primitive condi-
tion, illustrated by the autapomorphic, relatively
long metacarpals of Pan. Ignoring the Miocene fossil
record obscures potentially critical information, and
new fossils will certainly help answer the questions.
Do the derived traits of A. afarensis
reflect bipedality?
Because there is such an extensive literature on
this subject, I will not review it here. Derived trait
lists and discussions of their significance can be
found in McHenry (1994) and Stern (2000), and are
reviewed in Aiello and Dean (1990). The skull, ver-
tebral column, pelvis, and entire lower limb all re-
flect clear and unambiguous characters recognized
as adaptations for upright, bipedal progression by
numerous mechanical analyses. They are all traits
shared at least to some extent with humans, the
only bipedal hominoids. These changes and their
similarities to modern humans are far more exten-
sive than the differences due to retained primitive
characters. This suggests that they were indeed ad-
aptations shaped by natural selection for bipedal
posture 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
198 YEARBOOK OF PHYSICAL ANTHROPOLOGY
retained features presumed to be adaptations for
arboreality compromised bipedal locomotion.
Some researchers have implied that the gait of A.
afarensis differed from that of humans because they
had slightly different limb proportions, muscle at-
tachment sites, and a pelvis with less coronally ori-
ented iliac blades and a smaller anterior horn of the
acetabulum than do humans. Some have suggested
that this indicates the bipedal gait of A. afarensis
was more energetically expensive than that of hu-
mans, or at least different (Berge, 1991; Cartmill
and 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 Australopithecus
might have looked different when it walked than do
extant humans (Jungers, 1984; Rak, 1991; Schmitt
et al., 1996; Ruff, 1998; Schmitt et al., 1999), it
remains to be demonstrated that they were less
capable bipeds, or if they differed from us, exactly
how. If Australopithecus could not walk as fast, far,
or well as do humans, and this was because of the
retention of traits that enhanced arboreality, then
this would support the hypothesis that stabilizing
selection had acted to maintain at some level of
arboreal competence.
Abitbol (1995) argued that A. afarensis had a low
sacral promontory angle between its lumbosacral
joint surface and anterior sacral body (70° in AL
288-1, compared with his reported range of 44 –56°
for humans, which I think is a likely underestimate
of variability, as I have a human skeleton with an
angle of 67°). He argues that this would necessitate
having their sacrum and pelvis in a more vertical
position than is typical for humans. This difference
in sacral angle could be accommodated by the less
anteriorly curved morphology of the sacrum, how-
ever, certainly when combined with a lumbar lordo-
sis, allowing the lumbosacral joint to lie in the same
plane as that of humans despite the different sacral
angle. A. afarensis certainly had a significant lum-
bar lordosis, as it has a wide lumbar interfacet dis-
tance between the presumed second lumbar and
first sacral vertebrae (Fig. 4). Increasing interfacet
distances allow the articular processes to imbricate,
minimizing the probability of developing spondylol-
ysis and spondylolisthesis (Latimer and Ward,
1993). Because significant posterior wedging of the
vertebral bodies occurs only in the last four lumbar
vertebrae (Fig. 4) (Latimer and Ward, 1993), the fact
the second lumbar vertebra preserved in AL 288-1 is
not wedged is irrelevant. A lumbar lordosis indicates
habitual 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. afarensis
gait was kinematically distinct from that of humans,
and that they walked with their hips and knees in a
more flexed posture (Susman et al., 1984; Preuschoft
and Witte, 1991; Stern, 1999). A bent-knee gait is
[Vol. 45, 2002
Fig. 4. Distance between superior zygapophyseal facet joints
in caudal eight vertebrae of Homo sapiens with 5 and 6 lumbar
vertebrae, 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 reflects
presence of a lumbar lordosis, as it allows zygapophyses to slide
past 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).
unlikely from a kinematic perspective, however, as
demonstrated by Crompton et al. (1998) and Kramer
and Eck (2000) using modeling. They demonstrated
that the lower limb length and conformation of AL
288-1 would not have produced a less energetically
efficient gait than in modern humans at walking
speeds, and Kramer and Eck (2000) even suggested
they might have even been more efficient. Kramer
and Eck (2000) argued that the preferred transition
speed from walking to running would have been
lower in A. afarensis than in humans. They went on
to suggest that this would have affected distance of
travel or day range, although there appears to be no
reason to assume any effect on day range based on
their analysis.
Ruff (1998) and Rak (1991) both argued that the
anatomy of AL 288-1 could only be explained if A.
afarensis walked with greater pelvic movements
than do modern humans, although neither of them
proposes a bent-hip-and-knee gait. AL 288-1 has
femoral head dimensions expected for a hominin of
her size (McHenry, 1991; Ruff, 1998), and her fem-
oral diaphysis is even stronger. However, because of
this, coupled with her longer femoral neck, Ruff
(1998) suggested that A. afarensis pelvic movements
during gait would have had to be greater because of
greater predicted hip and femoral strains. Because
his analysis of mediolateral bone strength was made
in relation to anteroposterior strength, the fact that
A. afarensis seems to have had proportionally stron-
ger bones throughout its skeleton (Ruff, 1998; Coff-
ing, 1998) could confound his comparison. It is also
Ward] INTERPRETING A. AFARENSIS LOCOMOTION 199

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

unclear why A. afarensis would have a very large
bicondylar angle in this situation. Still, Ruff (1998)
did not argue for a bent hip posture. Rak (1991) also
posited greater pelvic movements, although in pelvic
rotation rather than lateral elevation. Neither of
these situations was modeled by Crompton et al.
(1998) or Kramer and Eck (2000), and they both
differ from one another. So, although there have
been main arguments made for a kinematically dis-
tinct gait, there is still no consensus on how their
gait differed, or what the costs in energy expendi-
ture or mobility would have been.
A bent-knee posture is also inconsistent with the
distal femoral morphology of A. afarensis. The ex-
panded calcaneal tuberosity of A. afarensis indicates
that initial contact during gait was a heel strike (see
also, Gebo, 1996), and that weight was borne on a
single support limb (Latimer and Lovejoy, 1989).
Heel strike would have occurred with the knee at or
near full extension, as it in humans, and the knee
would have been straightened further through mid-
stance and late stance. The lateral lip of the patellar
groove is higher than the medial one in both A.
afarensis specimens AL 129-1 and AL 288-1, and
differs markedly from the situation seen in apes,
despite the mediolaterally broad distal femur re-
tained in A. afarensis (Fig. 5). AL 288-1 is slightly
damaged along its superior patellar surface, which
often cannot be appreciated on casts. This elevated
surface is consistent with the valgus angle, and with
significant quadriceps muscle contraction at or near
full extension, as would occur from initial contact
through 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 the
degree of femoral condylar flattening may not be as
extensive as in most adult modern humans, their
shape is fully human-like and resembles that of
modern 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 stereotypic
loading patterns of normal gait. Apes have nearly
circular condylar profiles, with similar joint con-
tours in all positions in the knee flexion-extension
cycle. This indicates that peak transarticular loads
occurred 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 this
results from a deepening of the patellar surface and
minimal overlap between the patellar and tibial
joint surfaces (Fig. 4). The tibial surfaces are re-
stricted to a posterior position, reflecting habitually
bent knees. Because A. afarensis individuals were
habitual bipeds, if the knee was adapted to being
loaded in partial flexion at heel strike, we should see
either no flattening, as muscular energy could be
used to dissipate ground reaction forces, or else any
flattening 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 rather
than different limb posture.
200 YEARBOOK OF PHYSICAL ANTHROPOLOGY
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 the
talar trochlea was more tightly curved than is that
of humans or gorillas, matching only chimpanzees
among extant hominoids. Furthermore, when range
of joint motion was estimated by articulating the
associated tibia, AL 288-1 had 2–3° greater range of
motion than seen in humans or gorillas (Stern and
Susman, 1983), which they interpreted as advanta-
geous for climbing in trees, suggesting arboreality in
A. afarensis. A new, larger talus from Hadar, AL
147-30 (unpublished findings), has a flatter trochlea
than that of AL 288-1, with a subtended angle of
only 115°, considerably less than that of AL 288-1,
which is 140° (Latimer et al., 1987). The new talus
falls within the human range (humans range from
95–120°, and chimpanzees from 110 –145°. This does
not necessarily indicate that large and small Hadar
hominids differ in locomotor repertoire, because
these individuals do not exceed the range of varia-
tion within extant species. Thus this new fossil re-
futes the hypothesis that the talocrural joint was
distinct from that of extant humans, although the
species range may have been lower. It is notable that
gorillas have a range of values from 90 –120°, like
humans, suggesting an allometric effect (Latimer et
al., 1987).
The relatively longer toes of A. afarensis (Stern
and Susman, 1983; Susman et al, 1984; White and
Suwa, 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 having
larger feet is uncertain. There are no associated
pedal and lower limb skeletons to assess relative
foot length empirically. Further, the variation
among extant humans with different relative foot
and toe lengths is considered normal intraspecific
variation, and few researchers would argue that any
humans 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 lower
limb posture was not within the range of modern
humans. Furthermore, the various analyses fail to
support a single mechanism by which they differ,
instead positing either different hip postures or
movement during locomotion. Data are unclear
whether 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 from
that of humans, there is no certainty that they
would have been less capable bipeds as a conse-
quence of their retained primitive traits. This then
begs the question of why Homo altered the primitive
hominin pattern, with its apparent mechanical im-
provements for bipedality. There are multiple possi-
[Vol. 45, 2002
bilities, which are largely beyond the scope of this
paper. Increasing body size may have played a part,
along with other selective pressures to modify pelvic
form to accommodate childbirth for larger-brained
infants (Tague and Lovejoy, 1986; Ruff, 1998). At
present, 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 not
enough to accurately assess change in patterns of
variation over time. It appears, however, that the
general pattern of postcranial morphology exhibited
within Australopithecus was essentially constant.
There is little evidence so far to suggest that Aus-
tralopithecus morphology continues to change over
time and become more human-like, although it is
possible 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 only
with the advent of Homo erectus/ergaster around 1.8
mya.
Within A. afarensis, the only taxon for which there
is even a hope of assessing temporal change (as in
craniodental material; Lockwood et al., 2001), there
is no apparent change over time postcranially. Com-
paring earlier and later Hadar specimens, there are
no apparent differences in postcranial form (but see
Senut, 1978, but see 1980; Tardieu, 1979, 1986a,b),
and certainly none identified so far to be outside the
range of variation exhibited in a modern species. No
other Australopithecus species has a sufficient num-
ber of specimens or temporal resolution to observe
potential change over time.
Across australopithecine taxa, there are only
weak hints of temporal trends to become less ape-
like and more human-like postcranially. The earliest
Australopithecus species identified so far is A. ana-
mensis (Leakey et al., 1995, 1998; Ward et al.,
1999a, 2001). Postcranially, A. anamensis is known
from only the proximal and distal thirds of a tibia, a
distal humerus, a nearly complete radius, and a
capitate and partial proximal manual phalanx. In
most 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 diaphysis
that 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). The
humerus, discovered long before it was attributed to
A. anamensis (Patterson and Howells, 1967), is in-
distinguishable from that of A. afarensis (Feldes-
man, 1982; Hill and Ward, 1988; Lague and
Jungers, 1996; Ward et al., 2001), despite sugges-
tions that it is more like that of Homo (Senut and
Tardieu, 1985; Baker et al., 1998), as is the phalanx.
The radius is similar as well, and belonged to a
Ward] INTERPRETING A. AFARENSIS LOCOMOTION
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 in
extant and fossil taxa (adapted from Latimer et al., 1987). All
hominins have vertically oriented tibial shafts relative to talar
joint surface, whereas apes have sharply inclined tibial shafts,
placing knee well lateral to ankle in terrestrial plantigrade pos-
ture.
forearm that was longer than the longest one pre-
served for A. afarensis (Heinrich et al., 1993). This
suggests that the forearms of A. anamensis were at
least as long as those of A. afarensis, and almost
assuredly longer for their body size than those of
Homo. The capitate is poorly preserved, but sug-
gests a more laterally facing second metacarpal
facet 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 the
capitate facet, reflecting rotational ability of the sec-
ond carpometacarpal joint (Leakey et al., 1998). Be-
cause it is likely that A. anamensis and A. afarensis
represent a single lineage, there is evidence of post-
cranial change only in the hand, but that bipedality
had been established by 4.2 million years ago. This
suggests that the primitive traits seen in A. afaren-
sis probably had been retained by bipedal hominins
for nearly a million years.
A. afarensis and A. africanus are similar postcra-
nially in overall morphological pattern, although
there are some comparatively minor differences
(Häusler, 2001 and references therein). When they
differ, A. africanus generally has slightly more hu-
man-like morphology than does A. afarensis, but not
201
always. Although their hands are strikingly similar
morphologically, A. africanus appears to have more
gracile metacarpal shafts and slightly straighter
phalanges with less well-developed flexor ridges
than does A. afarensis (Ricklan, 1987). There also
seems to be a large apical tuft on the pollical distal
phalanx. Although this bone is not known for A.
afarensis, the other A. afarensis distal phalanges
have narrow apical tufts (Bush et al., 1982). The A.
africanus pelvis appears to have had a slightly more
anteroposteriorly expanded inlet with a more sagit-
tally oriented iliac blades, with better-developed cra-
nial angles of the sacrum. This suggests a different
overall shape of the lower torso in each species.
Häusler (2001) reported on an indistinct iliofemoral
ligament attachment in A. afarensis compared with
a 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 in
both species. Häusler (2001) also showed that the
latissimus dorsi attachment site on the iliac crest is
more medially restricted in A. africanus, like mod-
ern humans, than in A. afarensis, suggesting less
powerful upper limbs in the Sterkfontein hominins.
There are several other ways in which A. africa-
nus has been interpreted to be more primitive and
arboreal, however. Clarke and Tobias (1995) argued
that 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 OH8
in 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 Häusler (2001)
noted that upper limb length to acetabulum size
does not differ between two partial skeletons of A.
afarensis (Al 288-1) and A. africanus (STW 431).
Differences noted by McHenry and Berger (1998) in
associated skeletons reflect the relatively large ra-
dial head of A. africanus (Häusler, 2001).
In summary, A. africanus may have been slightly
more derived than was A. afarensis in most features
where the species differ. Because A. africanus is
later in time (McKee, 1993; Walter, 1994; McKee et
al., 1995), this could indicate a directional trend. If
these taxa represent a single lineage, this might
signal disaptation in the traits that change and their
related 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 the
same sites. The putative A. robustus hand bones are
described as more human-like, with broader apical
tufts on the terminal phalanges and flat first meta-
carpal bases (Susman, 1988, 1989). Its ilium (SK
3155) has been described as having a relatively
wider and more cranially extensive iliac blade with a
202 YEARBOOK OF PHYSICAL ANTHROPOLOGY
larger auricular surface than those of A. africanus
and A. afarensis (Brain et al., 1974; McHenry, 1975),
but this variation may reflect body size and/or indi-
vidual variation (McHenry, 1975). Other A. robustus
postcranial bones are not notably different from
those 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 the
Bouri Formation in Ethiopia cannot be definitively
attributed to A. garhi, the only hominin identified at
the site (Asfaw et al., 1999). However, these fossils
display a primitive, A. afarensis-like brachial index
but with a proportionately longer lower limb, sug-
gesting selection for increased lower limb length if
this hominin was a descendent of A. afarensis.
Thus, the basic pattern of postcranial anatomy
exhibited by A. afarensis appears to persist for over
3 million years, suggesting that its locomotor adap-
tation was stable, and not undergoing ongoing selec-
tion for improved terrestrial competence. The slight
differences between A. africanus and A. afarensis
might signal slight directional selection towards a
Homo-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 limb
elongation may have occurred. These observations
are speculative, and meant only to point out possi-
bilities. If they were eventually supported by further
evidence, 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 retained
seems to be the strongest evidence that primitive
morphology retained an adaptive advantage for Aus-
tralopithecus individuals, although it does not fal-
sify the null hypothesis of nonaptation. If bipedality
began with late Miocene putative hominins like Sa-
helanthropus and Orrorin, both about 6 million
years old, it would have been around for 3 million
years before the appearance of A. afarensis. Even so,
it had been around for almost 1 million years since
A. anamensis. The general australopithecine body
plan 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 or
alter them. If they were selectively neutral, we need
to explain why they never changed until the appear-
ance of Homo.
Did A. afarensis actually climb trees?
Another question to address would be whether or
not we have enough evidence to assess whether A.
afarensis was actually climbing trees or not. This
would be important to reconstruct behavior, and to
[Vol. 45, 2002
perhaps hint at the evolutionary significance of ar-
boreality. Relatively few studies have investigated
this possibility. Data about actual behaviors will
come from traits that are phenotypically plastic, and
reflect 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; Ruff
et 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 they
actually traveled bipedally. The pronounced femoral
bicondylar angle indicates that A. afarensis actually
engaged in bipedal walking or running (Tardieu and
Trinkaus, 1995; Duren, 1999). The flattened femoral
condyles may also reflect habitual loads in knee
extension, as joints appear to be shaped during
grown by response to hydrostatic pressure in artic-
ular cartilage (Frost, 1990a; Hamrick, 1999). Evi-
dence for tree-climbing is less clear, but also not
thoroughly explored.
Coffing (1998) examined metacarpal diaphyseal
robusticity in Australopithecus and extant homi-
noids. She argued that skeletal changes improving
terrestrial competence in A. afarensis would have
decreased their arboreal capabilities. She predicted
that if A. afarensis still practiced arboreal behaviors,
they would have to have had even greater forelimb
strength than extant apes. She did not explicitly
discuss issues of genetic vs. epigenetic effects on
diaphyseal form, but given assumptions about bone
modeling, it was implicit that individual behaviors
were involved. Her analyses suggested that A. afa-
rensis did indeed have stronger metacarpal diaphy-
ses than would be expected for their body size and
bone lengths compared with those of modern hu-
mans. Ruff (1998) reported that the femur was also
more robust than humans or apes, however, sug-
gesting that their skeletons were more robust over-
all than the modern taxa, rather than being tied to
arboreality or bipedality. Still, this provides some
indirect support for Coffing (1998). Coffing (1998)
implied that her hypothesis is mainly about upper
limb strength, but it could be interpreted to mean
strength 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 et
al., 1984), and the peroneal groove on the fibula and
peroneal trochlea on the calcaneus (Latimer and
Lovejoy, 1989, 1990b). Indicators of relative muscu-
larity in all regions of the A. afarensis skeleton are
generally greater than in modern humans, as with
all premodern hominins (Ruff et al., 1993, 1999;
Coffing, 1998). If overall muscularity was greater in
A. afarensis than in modern humans, it would not be
possible to test whether this was to improve climb-
Ward] INTERPRETING A. AFARENSIS LOCOMOTION
ing specifically, or for other reasons such as foraging
or defense.
Richmond (1998) and Paciulli (1995) conducted
cross-sectional growth studies of phalangeal curva-
ture in apes and humans. They both found that
curvature is greatest during the juvenile period,
roughly at the time in which juveniles spend the
greatest proportional amount of time engaging in
arboreal behaviors. If their results are confirmed by
other analyses, particularly longitudinal ones, this
would be a character indicating that at least juvenile
A. afarensis spent time in the trees. Contrary to the
results of phalangeal studies, Tardieu and Preuschoft
(1996) inferred that the morphology of developing
epiphyseal plates was affected by behavior, and that
the immature Hadar femora resemble those of hu-
mans, and not apes. This suggested to them that A.
afarensis individuals were not climbing, as they
lacked the apparent adaptations for stabilizing the
epiphysis during arboreality. Duren (2001) also
found 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 humeral
torsion (Martin and Saller, 1959; King et al., 1969;
Sarmiento, 1985; Pieper, 1998). As noted above,
Australopithecus has less humeral torsion than do
humans or extant great apes. This could be inter-
preted as a series of evolutionary reversals or char-
acter transformations from an ape-like ancestor to
Australopithecus to human. However, this feature
may well be epigenetically influenced, as captive
and 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 torsion
than other people. Because humeral torsion also is
influenced structurally by scapular position and el-
bow joint orientation, via whatever mechanisms, the
fact that A. afarensis differs from humans and ex-
tant apes in having less torsion could be related to
the inferred different shape of their thorax (Schmid,
1983; Jellema et al., 1993). Thus, lower humeral
torsion in A. afarensis could represent structural
differences 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 of
Australopithecus, we can consider the capabilities
evident in their morphology. Even if A. afarensis
spent time in the trees, without a grasping hallux
(White and Suwa, 1987; Latimer and Lovejoy,
1990b; but see Clarke and Tobias, 1995) they would
have been significantly less agile than are apes and
monkeys, especially in the case of females holding
infants. Despite the apparently slightly longer and
more curved toes than are typical for modern hu-
mans, their toes were still shorter and straighter
than those of apes (Bush et al., 1982; Latimer and
203
Lovejoy, 1990b; Stern and Susman, 1983; White and
Suwa, 1987), and so the size of supports they could
have grasped would be less. Even if their manual
grasp was greater than that of humans, and their
pedal grasp like that of the manual grasp of modern
2-year-old humans (Susman et al., 1984; Stern,
2000), we still cannot be sure that this was retained
for adaptively significant arboreal behaviors. They
would have been more competent in the trees than
are typical humans, as they are much stronger and
had very slightly better mechanics with longer
arms, fingers, and toes. Any arboreal locomotion
would still necessarily have been fairly slow and
deliberate, however, more for something like sleep-
ing in trees than for hunting or fleeing from preda-
tors. Certainly females with infants would have had
difficulty climbing trees, because without grasping
halluces they would have had to hold onto their
infant with at least one arm. Still, sleeping in trees
for 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 sensitive
morphology have shown that A. afarensis individu-
als walked bipedally, but do not lead to a consensus
about A. afarensis locomotion. Relatively few studies
have been conducted so far, however. Research on
the influences of individual activity patterns on the
development of adult morphology is key to determin-
ing what behaviors A. afarensis individuals engaged
in over the course of their lifetime, and are well
worth 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 of
anatomy (recent discussions in Witmer, 1995;
Churchill, 1996; Lieberman, 1997, 1999; Lovejoy et
al., 1999, 2000). Of course, though all we have are
the bones of fossil animals, we need to bear in mind
that the growth and function of soft tissues can
influence skeletal form (Witmer, 1995, 1997). We
know 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 genetic
and 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 selection
for an aspect of one trait can directly impact the
form of another. This is not to say, however, that
selection cannot independently modify structures,
only that it is possible that structures may experi-
ence modifications concomitant with selection on a
linked trait. The functional and evolutionary signif-
icance of bone form can only be understood accu-
204 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 45, 2002
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 significant
differences in the positional information of its cells, and their resultant effects on pattern formation. Type 1 traits are fixed by
directional and/or stabilizing selection because their primary functional features have a real effect on fitness, and result largely
from a direct interaction between genes expressed during tertiary field deployment and the functional biology of their adult
product.
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 their
phenotype. Type 2 traits differ in two taxa because of differences in pattern formation (as in type 1), but their functional effect
is so minimal as to have had no probable real interaction with natural selection. Their principal difference from types 4 and 5
is 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” are
attributable 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 are
epiphenetic and not pleiotropic. However, they provide significant behavioral information, and are of expository or evidentiary
value 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 to
behavior. Such traits are not consistently expressed within species, and often show marked variation of expression within
individuals and local populations.

rately if the range of influences on it is elucidated.
The existence of these effects and their potential
consequences is not a new revelation, but has al-
ways been verging on unobtainable information, and
so by practical necessity is often ignored.
An example of integrated morphology is the shift
in overall torso shape in apes and monkeys (Benton,
1965, 1976; Ward, 1991, 1993). Great apes have
vertebral transverse processes that arise from the
neural arch rather than the vertebral body, flaring
iliac blades, and coronally oriented scapulae, along
with 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 related
with one another, and always correlated, they ap-
pear to represent related changes resulting from a
reorganization of the torso, in this case to enhance
the effectiveness of abduction-adduction movements
of the arm for arm-hanging and forelimb-dominated
arboreal activities.
Recent scientific progress is improving our ability
to incorporate pleiotropic and ontogenetic informa-
tion in paleontological interpretations. Discoveries
in the fields of genetics and developmental biology
have been rapidly increasing our knowledge about
the control and ontogenetic mechanisms of structure
formation (e.g., Hinchcliffe, 1991; Wolpert, 1983;
Hall, 1999; Cohn and Bright, 2000; Gilbert, 2000;
Skerry, 2000; Hamrick, 2002; other articles in
O’Higgens and Cohn, 2000). An interesting set of
examples of developmental genetic links among ap-
pendicular and axial structures comes from studies
of Hox genes, as well as other gene systems such as
Pax. Alterations in their expression appear to affect
the condensation and proliferation of limb-bud mes-
enchyme, and mutations in these genes generally
have 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 and
Hoxa-13 mutations can result in reduction of the
first ray and increased length of rays 2–5, mirroring
changes thought to have occurred in apes. Hoxd-11
can be responsible for a suite of alterations, includ-
ing reduced metacarpals 2–5, reduction of the ulnar
styloid 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 of
morphologies appears to differentiate hominins
from apes, suggesting the possibility of a single ge-
netic change resulting in multiple developmental
shifts. The extent to which a single gene is involved
remains to be determined, but pleiotropy is a tena-
ble hypothesis. As the details of these links and their
effects on adult form continue to be worked out, it is
critical that we incorporate this type of information
into our morphological and phylogenetic interpreta-
tions.
The most explicit attempt to assess and code the
types of interaction among tissues and structures
via ontogeny and selection in determining form has
been that of Lovejoy et al. (1999, 2000). They pro-
posed five trait types that differ in the degree to
which they are acted upon directly or indirectly by
selection, are influenced by selection on related
structures, or are epigenetically influenced by indi-
vidual activity over a lifetime (Table 1). This classi-
fication system represents a model to employ when
attempting to interpret evolutionary history or be-
havior in fossil taxa, and so should be useful for
assessing Australopithecus. By employing either
this system, or at least the logic underlying it, we
should be in a better position to more accurately
interpret early hominin morphology.
The difficulty will often be in identifying the spe-
cific influences on a trait, and classifying individual
traits, as illustrated by some of the examples in
Lovejoy et al. (1999, 2000). In addition, some char-
acters may fall into more than one type category,
Ward] INTERPRETING A. AFARENSIS LOCOMOTION
having multiple influences, and so perhaps sending
us multiple signals. Still, using this general ap-
proach, we can construct testable hypotheses about
the 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 the
comparative method. The importance of this scheme
lies in its attempt to identify the influences on bone
form.
An excellent example of a trait whose influences
currently are under intense scrutiny is long bone
diaphyseal form. One bone mechanical theory states
that certain levels of strain trigger bone-modeling
responses, as bone models to maintain particular
strain distributions necessary to perform necessary
metabolic function while maintaining structural in-
tegrity (Martin et al., 1998 and references therein).
Using engineering beam theory, investigators have
inferred that because bones are subjected to bending
under normal physiological loading conditions, the
greatest tensile strain caused by bending should be
located near midshaft. Tensile strain is thought to
invoke the most significant modeling response in
bone. Operating on the assumption that bone mod-
els to minimize tissue strain, researchers inferred
that the plane in which maximum bending occurs
should have the greatest bending rigidity. Thus, the
amount of load to which a bone is subjected during
growth should be reflected in its midshaft diaphy-
seal cross-sectional geometry. This assumption was
used to infer activity patterns in humans and other
primates (Ruff, 2000; Martin et al., 1998).
As this field of inquiry developed, it was gradually
realized that other variables such as body shape are
influential in determining long bone form. It cer-
tainly is becoming apparent that there is an age
effect on the responsiveness of bone to activity pat-
tern, because mechanical sensitivity of the modeling
response appears to diminish as an individual ap-
proaches skeletal maturity (Frost, 1990a, b; Carter
and Beaupré, 2001). Furthermore, some experimen-
tal strain gauge work suggests that contrary to the
assumptions used to infer habitual direction of
bending strain in long bones, the plane of greatest
bending rigidity may not always be the same as the
plane of greatest bending strain, at least during
loads incurred by walking or climbing (Demes et al.,
1998, 2001). It may be that patterns of muscle re-
cruitment, when counteracting ground reaction
forces, may exert more relevant strain distributions
rather than simply the ground reaction vectors.
However, the one animal that galloped in the study,
incurring maximum strain values, did have peak
strains that approached the orientation predicted by
bone sectional form (Demes et al., 2001). This may
suggest 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 when
using cross-sectional diaphyseal form to infer behav-
205
ior. They also suggest that different bones have dif-
ferent constraints on their form. Most recently, it
was proposed that epiphyseal plate form is a greater
determinant of diaphyseal cross-sectional form than
is activity (Ohman and Lovejoy, 2001). Data sug-
gest, however, that while within some taxa there
may be an effect of epiphyseal geometry on diaphy-
seal midshaft shape, there is considerable variation
in this relationship, and it does not hold true within
or among taxa in metacarpals (Holden and Ward,
unpublished data) or femur (Nalley and Ward, un-
published data). It appears now that there may be
an inherent, genetically influenced initial shape de-
termined in part by selection on joint form, which
influences epiphyseal geometry. This geometry may
have a slight effect in diaphyseal cross-sectional
form. This initial form then may be modified by
activity pattern (Martin et al., 1998 and references
therein), especially early in life (Ruff et al., 1994).
Body proportions and muscle distributions about the
bone affect patterns of bone strain, and ultimately
diaphyseal form. It also appears that bone may not
model to eliminate strain, but to enhance predict-
ability of strain, and even to maintain a certain level
of strain with activity (Bertram and Biewener, 1983;
Rubin, 1984). According to the scheme of Lovejoy et
al. (1999, 2000) (Table 1), long bone diaphyseal form
appears to be a mixture of trait types 1, 2, and 4.
The picture is complex, but this attention to the
determinants of diaphyseal form is exactly what is
needed to determine the genetic and epigenetic in-
fluences on bony morphology, and any other ontoge-
netic or pleiotropic effects. Armed with such detailed
information, we will be better able to accurately
infer activity patterns from the skeleton. We will
also be in a better position to use morphological
information to infer phylogeny and interpret pat-
terns of character transformation within a lineage.
Again, advances in our understanding of genetic
and other molecular influences on the development
of adult form will help us develop and test more such
hypotheses, and improve the accuracy with which
we interpret the fossil record.
IMPLICATIONS FOR TESTING HYPOTHESES
ABOUT 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 to
determine what A. afarensis individuals looked like
and what they did, and how they evolved over time,
provides the raw data with which to test hypotheses
about relationships between locomotion and other
aspects of a species’ biology, such as diet or social
behavior.
Since many hypotheses proposed to explain the
evolution of bipedality revolve around diet and food
acquisition (Du Brul, 1962; Hunt, 1994; Jolly, 1970;
Prost, 1980; Wrangham, 1980; others summarized
by Rose, 1991; Richmond et al., 2001), it is worth
considering links between the adoption of Australo-
206 YEARBOOK OF PHYSICAL ANTHROPOLOGY
pithecus bipedality and evidence of diet. A. anamen-
sis exhibits different dentognathic morphologies
from those of earlier hominoids, and so appears to
have had a different dietary specialization. A. ana-
mensis shares thick enamel on its teeth with all
later 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 stronger
than that of apes, and less robust that that of later
hominins (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 differs
slightly from that of apes. Thus there appear to be
changes in diet associated with Australopithecus,
and thus far, with committed bipedality. Teaford
and 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 necessarily
dependent on one another in some fashion, we might
expect to see them associated in some consistent
pattern across bipedal hominins. While there appear
to be concomitant dietary and locomotor changes
associated with the origin of Australopithecus, there
is no such evidence within the genus. The evidence
is extremely sparse from which to make such assess-
ments with any confidence so far. Still, from what
little is preserved, evidence of dietary diversity
among Australopithecus species does not, so far, ap-
pear to be associated with a consistent pattern of
locomotor specializations. A. africanus had slightly
larger 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 more
human-like than A. afarensis in some features, al-
though there is little overall difference.
A. garhi had large molars like those of robust
australopithecines, a large sagittal keel, and other
intense chewing adaptations (Asfaw et al., 1999). If
the postcranial elements from the same site are
indeed those of A. garhi, it would appear to differ
from other Australopitheci postcranially as well,
with more human-like limb proportions than the
other species for which this can be determined. The
only associated A. boisei postcranial fossil associated
with cranial remains is KNM-ER 1500. This fossil is
poorly 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-object
feeding specialization and more human-like propor-
tions. A. robustus, however, shows only slight evi-
dence for such an association. Since all postcrania
attributed to A. robustus are isolated, proportions
are difficult to assess. Two ulnae are unassociated
with any craniodental material, but have been ten-
[Vol. 45, 2002
tatively referred to robust Australopithecus: Omo
L40-19 (Howell and Wood, 1974; McHenry, 1976;
Day, 1978; Feldesman, 1979; McHenry and Te-
merin, 1979) and Olduvai OH 36 (Walker and
Leakey, 1993; Aiello et al., 1999). They appear more
curved than do those of A. afarensis and A. africa-
nus, or of those of Homo, and their proximal ends
also have some ape-like characteristics (Drapeau,
2001). It is not yet clear, however, whether the hy-
pothesis can be falsified that the variation exhibited
by all Australopithecus ulnae exceeds that found in
any single extant species, much less genus.
In summary, the heavy chewing adaptations seen
in A. garhi and other robust Australopithecus spec-
imens do not appear to be systematically linked with
more human-like skeletons, although there may be a
slight association. Admittedly, postcranial fossils
are poorly known for most Australopithecus species.
As more are discovered, this picture may change. At
present, however, while dietary adaptation may well
have accompanied the origin of Australopithecus,
from the limited data available, diet does not appear
to be an exclusive correlate of locomotor adaptation
among early hominins. Because of the poor fossil
record of postcranial anatomy of most Australopithe-
cus species, any such conclusions must remain ten-
tative at present.
Other hypotheses suggest that social behavior is
linked with the acquisition of terrestrial bipedality
(Lovejoy, 1981; Jablonski and Chaplin, 1993; others
summarized by Rose, 1991). One way in which social
behavior can be reflected in the fossil record is in
sexual 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 high
levels of sizes represented in all species of Australo-
pithecus for which this is measurable (reviewed in
Plavcan, 2000, 2001). No monogamous extant pri-
mate species has this much size dimorphism. All
extant taxa with this much body size dimorphism
are polygynous, either living in single- or multimale
groups, but with fairly intense levels of male-male
competition (Plavcan, 2000, 2001). Hence, while it is
clear that relatively large canines had ceased to
confer reproductive advantage to male hominins,
body size was apparently still valuable. Thus, the
data do not support an association between monog-
amy and bipedality. The data do offer a link between
the cessation of canines as useful weapons in male-
male competition and the origins of committed bipe-
dality, however. Furthermore, this extreme body
size dimorphism differs from the pattern seen in
humans and Pan, which all have much lower levels
of body mass dimorphism. Pan retains significant
canine dimorphism, while humans do not. The data
suggest that Australopithecus social systems dif-
fered from those seen in chimpanzes, bonobos, or
humans. Similarities in social behavior shared be-
tween humans and chimpanzees on the one hand
Ward] INTERPRETING A. AFARENSIS LOCOMOTION
(Wrangham, 1999), and humans and bonobos on the
other (Zihlman et al., 1978), appear to have evolved
independently.
The nature of early hominin bipedality, and of
potential 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 to
bipedality, 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 have
been acquired independently.
Other hypotheses about early hominin behavior,
of which there are many, are not directly testable
using 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 the
origins of bipedality by providing potentially new
associations between locomotor, dietary, and social
behavioral adaptations in early hominins. They will
also provide important information on the direction
of 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 data
on hominin evolution, our theoretical approaches
govern how we interpret them. The debate over lo-
comotion in Australopithecus as it has been framed
so far is becoming ineffective for helping us under-
stand early hominin locomotor evolution. By identi-
fying the causes of this debate and reframing the
questions we ask of the fossils, we are in a better
position to make progress. Some researchers have
been concerned with attempting to reconstruct the
selective regime that shaped A. afarensis, or why it
evolved as it did. Others have been more concerned
with reconstructing individual activity patterns, or
what they were like. Both approaches have value for
developing a more complete understanding of the
early radiations of hominins. We also need to remain
aware that some details about both research ques-
tions will be beyond the limit of resolution allowed
by the fossil record.
By clearly acknowledging the questions we are
asking about the fossils, we can then use the data
available to develop tests of hypotheses about adap-
tation and/or behavior. Studies of adaptation must
start with a reliable phylogeny incorporating living
and 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 whether
primitive retentions were retained by stabilizing se-
lection for maintenance of an ancestral behavior,
like climbing trees, we must determine whether the
primitive morphology compromised the derived
207
function. If this is not possible, we can try to use
evidence of stasis or reconstructed behaviors to give
us hints about the extent of stabilizing selection.
Disaptation can be disproven by the continued
maintenance or enhancement of a structure. To test
hypotheses about which behaviors A. afarensis indi-
viduals engaged in, we can consider the selective
regime suggested by their apomorphic morphology,
but we also must attempt to identify traits that are
epigenetically sensitive to activity patterns.
Using this investigative framework, what we can
infer 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 to
be habitual terrestrial bipeds. This hypothesis is
supported 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 to
modern hominin bipeds. Furthermore, epigeneti-
cally sensitive traits, such as femoral bicondylar
angles and epiphyseal contours, indicate that A. afa-
rensis actively engaged in bipedal locomotor behav-
iors. Arboreal competence was reduced, indicating
that arboreality was of diminished importance for
individual survival and reproductive success. Most
adaptations for arboreality likely present in the last
common ancestor of apes and humans were altered
or lost. None was enhanced in response to changes
favoring bipedality, except perhaps for an increase
on overall strength (Coffing, 1998). Clearly, the re-
productive consequences of habitual bipedal travel
were considerable.
Moreover, the massive rearrangement of bone and
joint 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). Their
ability to climb trees is more important to them in
terms of reproductive success, however, so apes have
not been selected to modify their skeletons to be-
come better bipeds. The selective consequences of
problems that might stem from a musculoskeletal
system poorly designed for bipedality, such as back
problems or joint pain, are minimal in very short-
distance locomotor bouts. On the other hand, the
fitness of an animal traveling longer distances more
regularly, at high speed, or for particularly repro-
ductively valuable reasons (e.g., inter- or intraspe-
cific competition, or carrying), would be in jeopardy
with any such maladies. For this reason, the only
scenario that would select for the major alterations
hominins underwent is if bipedality was employed
for more than simply standing and feeding, or walk-
ing very short distances. The adaptive importance of
bipedal travel is highlighted by the loss of the many
advantages of arboreal traits, in particular a grasp-
ing hallux, for use in climbing trees with speed and
208 YEARBOOK OF PHYSICAL ANTHROPOLOGY
agility for feeding, hunting, or predator escape, or
for infants being able to cling to their mothers’ fur.
This is not to say that using trees to some extent
was not necessarily selectively valuable for A. afa-
rensis, but this assumption is difficult to test. It is
almost certain that A. afarensis individuals would
have been more capable climbers than are most
modern humans. They were smaller and relatively
stronger. They retained primitive features, such as
slightly longer arms, hands, and feet, that would
have made them slightly more competent in the
trees than are modern humans, but still consider-
ably less so than any ape. The issue is whether or
not these features were actively maintained for
climbing by causing individuals who lacked them, or
in whom they were more poorly developed, to leave
fewer descendents than those who did. Particularly
in light of the strong directional signal away from
arboreality towards bipedality, it is difficult to dis-
prove the null hypothesis that these traits remained
as secondary nonaptations. There is no conclusive
evidence yet that the retained features of Australo-
pithecus compromised its effectiveness as a biped,
but many researchers support this idea. The shape
of the femoral condyles and the bicondylar angle do
not support the hypothesis that Australopithecus
walked with a bent knee and hip, a position further
supported by modeling.
The strongest support for a hypothesis of stabiliz-
ing selection at the moment is the apparently long
period 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 a
slight trend toward more “human-like” anatomy
over time prior to 1.8 million years ago, and even
this is a very tentative observation.
What we can say about the behavior of A. afaren-
sis is that they were habitual bipeds, based on trait
polarities 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 to
support or refute this hypothesis. The robusticity of
their skeletons may also prove to be related to arbo-
real behaviors, but this has not been clearly demon-
strated yet. Studies of kinematic characteristics of
A. afarensis gait patterns have produced conflicting
results. Continued elucidation of the genetic, devel-
opmental, and epigenetic bases for morphological
features and character complexes will be of critical
importance in testing hypotheses about the actual
day-to-day behaviors of Australopithecus individu-
als. This will also help us explore the current uses to
which primitive traits of A. afarensis were put. In
addition, these data will help us make more accu-
[Vol. 45, 2002
rate phylogenetic reconstructions by allowing us to
make more appropriate character choices for our
analyses.
The extent to which A. afarensis was arboreal has
implications for interpreting the pattern of natural
selection that shaped the early part of our lineage.
Recent claims for locomotor diversity among early
hominin species (Berger and Tobias, 1996; Clarke
and Tobias, 1995; McHenry and Berger, 1998) and
the 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 hominin
positional behaviors. In addition, our understanding
of Australopithecus locomotor behavior is important
for understanding the transition to Homo. If austra-
lopithecines and other early hominins were partly
arboreal, 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 were
already fully bipedal, the changes in the Homo skel-
eton must have been due to other factors, such as an
increase in efficiency due to walking longer dis-
tances or running, and/or selection for body size,
throwing, tool use, and transport, or any number of
other possibilities. Until we find a way to resolve
this ongoing debate over the importance of arbore-
ality in A. afarensis and other early hominins, we
will have a difficult time characterizing the impor-
tant transition (or transitions) involving postcranial
anatomy that shaped our lineage.
ACKNOWLEDGMENTS
I thank Dave Begun, Mark Collard, Deborah Cun-
ningham, Michelle Drapeau, Mark Flinn, Anne
Holden, Amy Judd, Bill Kimbel, Bruce Latimer, Thi-
erra Nalley, Jason Organ, Brian Richmond, and
Alan Walker for helpful discussions about the con-
cepts in this paper and sharing information. I thank
Lee Berger, Ron Clarke, Don Johanson, Bill Kimbel,
Bruce Latimer, Meave Leakey, Steve Leigh, Brian
Richmond, Philip Tobias, and the staffs of the Cleve-
land Museum of Natural History, National Muse-
ums of Kenya, the Transvaal Museum, National
Museums of Ethiopia, the University of the Witswa-
tersrand, and the Institute of Human Origins for
access to fossil, comparative skeletal, and cadaver
specimens. I also thank Chris Ruff for inviting me to
contribute this manuscript, and Martin Häusler,
Dan Lieberman, Henry McHenry, Chris Ruff, and
an anonymous reviewer for helpful comments and
suggestions.
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