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Interpreting the Posture and Locomotion of

Australopithecus afarensis: Where Do We Stand?

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- or lost. To infer the behaviors of a fossil species, we must
ity is key to understanding early hominin evolution. Be- first determine its adaptations, use this to make hypoth-
cause it is the best-known early hominin species, Austra- eses about its behavior, and test these hypotheses using
lopithecus afarensis forms a baseline for interpreting epigenetically sensitive traits that are modified by an
locomotion in all early hominins. While most researchers individual’s activity pattern. When the A. afarensis data
agree that A. afarensis individuals were habitual bipeds, are evaluated using this framework, it is clear that these
they disagree over the importance of arboreality for them. hominins had undergone selection for habitual bipedality,
There are two main reasons for the disagreement. First, but the null hypothesis of nonaptation to explain the re-
there are divergent perspectives on how to interpret prim- tention of primitive, ape-like characters cannot be falsified
itive characters. Primitive traits may be retained by sta- at present. The apparent stasis in Australopithecus post-
bilizing selection, pleiotropy, or other ontogenetic mecha- cranial form is currently the strongest evidence for stabi-
nisms. Alternately, they could be in the process of being lizing selection maintaining its primitive features. Evi-
reduced, or they simply could be selectively neutral. Sec- dence from features affected by individual behaviors
ond, researchers are asking fundamentally different ques- during ontogeny shows that A. afarensis individuals were
tions about the fossils. Some are interested in reconstruct- habitually traveling bipedally, but evidence presented for
ing the history of selection that shaped A. afarensis, while arboreal behavior so far is not conclusive. By clearly iden-
others are interested in reconstructing A. afarensis behav- tifying the questions we are asking about early hominin
ior. By explicitly outlining whether we are interested in fossils, refining our knowledge about character polarities,
reconstructing selective history or behavior, we can de- and elucidating the factors influencing morphology, we
velop testable hypotheses to govern our investigations of will be able to progress in our understanding of the pos-
the fossils. To infer the selective history that shaped a ture and locomotion of A. afarensis and all early hominins.
taxon, we must first consider character polarity. Derived Am J Phys Anthropol 45:185–215, 2002.
traits that enhance a particular function, are found to be © 2002 Wiley-Liss, Inc.
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
Grant sponsor: NSF; Grant number: SBR 9601025; Grant sponsor:
traits is that of selective neutrality, or nonaptation. Dis-
University of Missouri Research Council and Research Board.
proving this requires demonstration of active stabilizing
or negative selection (disaptation). Stabilizing selection
*Correspondence to: Carol V. Ward, Department of Anthropology,
can be inferred when primitive traits compromise a de- and Department of Pathology and Anatomical Sciences, 107 Swallow
rived function clearly of adaptive value. Prolonged stasis, Hall, University of Missouri, Columbia, MO 65211.
continued use of the trait for a particular function, or no E-mail:
change in variability in the trait are evidence that can
support a hypothesis of adaptation for primitive traits, but DOI 10.1002/ajpa.10185
still do not falsify the null hypothesis. Disaptation, or Published online in Wiley InterScience (www.interscience.wiley.
negative selection, should result in a trait being reduced com).


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


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-

tense in the early 1980s, after the publication of the
Bipedality is the hallmark of the human lineage. Hadar fossil descriptions, and it continues to this
Whether or not our unique locomotor mode evolved day. Some researchers have presented data support-
in the original members of our clade, it represents a ing the hypothesis that Australopithecus afarensis
fundamental adaptive shift away from the apes. Bi- individuals were obligate bipeds for whom arboreal-
pedality has served as a significant preadaptation to ity was adaptively insignificant (Lovejoy et al., 1973;
the acquisition of other key human characteristics, Lovejoy, 1975, 1978, 1988; Day and Wickens, 1980;
such as tool-making, altriciality of infants, and ar- White, 1980; Latimer, 1983, 1991; Ohman, 1986;
guably even intelligence. Understanding the nature Latimer et al., 1987; Latimer and Lovejoy, 1989,
and timing of the transition to terrestrial bipedal 1990a, b; Crompton et al., 1998; Kramer, 1999).
locomotion is key to an accurate interpretation of Others contend that A. afarensis was primarily bi-
how and why humans evolved. pedal, yet retained significant adaptations to arbo-
Over the past 78 years, our knowledge of the na- reality and thus was partly arboreal (Senut, 1980;
ture of early hominin (which I define as members of Stern and Susman, 1981, 1983, 1991; Feldesman,
the human clade more closely related to us than to 1982; Jungers, 1982, 1991; Jungers and Stern, 1983;
Pan; see Richmond et al., 2001) bipedality has im- Schmid, 1983; Rose, 1984, 1991; Susman et al.,
proved dramatically. Dart (1925) correctly inferred 1984; Deloison, 1985, 1991, 1992; Tardieu 1986a, b;
that the Taung child had upright posture, and that Susman and Stern, 1991; Duncan et al., 1994; Stern,
bipedality characterized the earliest part of the hu- 2000), perhaps with a compromised form of bipedal
man lineage. This interpretation was bolstered by progression stemming from these retained arboreal
further early hominin fossil finds, particularly in characters (Susman et al., 1984; Preuschoft and
South Africa, over the next few decades (e.g., Broom, Witte, 1991; Rak, 1991; Cartmill and Schmitt, 1996;
1943; Broom and Schepers, 1946; Le Gros Clark, MacLatchy, 1996; Schmitt et al., 1996, 1999; Ruff,
1947, 1955; Straus, 1948; Broom and Robinson, 1998; Stern, 1999). At least one researcher argued
1949, 1950; Dart, 1949a,b, 1958; Kern and Straus, that A. afarensis was not bipedal at all, but was a
1949; Broom et al., 1950; Mednick, 1955; Chopra, palmigrade-plantigrade quadruped (Sarmiento,
1962; Napier, 1964, 1967; Day and Wood, 1969; 1987, 1994, 1998). The debate is polarized and po-
Lovejoy and Heiple, 1970), with interpretations cul- larizing, and is to the point that it impedes our
minating in Early Hominid Posture and Locomotion further understanding of the posture and locomotion
(Robinson, 1972). With the discovery of earlier and of early hominins. It serves little further purpose as
more numerous Australopithecus afarensis1 fossils it has been framed thus far.
in the 1970s (Taieb et al., 1974, 1975; Johanson et Recently, even earlier hominins have been discov-
al., 1982b and references therein) and footprints at ered. Australopithecus anamensis is now known to
Laetoli (Leakey and Hay, 1979), research on Austra- have been a committed biped at 4.2 mya, but is
lopithecus locomotion intensified, and more detailed poorly known postcranially (Leakey et al., 1995,
questions began to be asked about the functional 1998; Ward et al., 1999a, 2001). Putative hominins
morphology of these 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-
Some researchers have suggested that because the genus Austra-
Selassie, 2001). From the limited data published so
lopithecus as traditionally defined may be paraphyletic or polyphyl-
etic, some species should be removed from Australopithecus and far, the nature of these hominins’ locomotor adapta-
placed in Praeanthropus or Paranthropus (Senut, 1996, 1999; refer- tions cannot be fully ascertained. Regardless of what
ences in Collard and Wood, 2000). Because this paper does not con- we learn about Sahelanthropus, Orrorin, and Ar-
sider the alpha taxonomy of hominins, and there is no general con- dipithecus in the coming years, Australopithecus,
sensus about hominin taxonomy, I will simply refer to all hominin
species originally attributed to Australopithecus (except Ardipithecus
and in particular A. afarensis, will remain the basis
ramidus) as a single genus, and focus my discussions on functional for our understanding of the origins and early evo-
interpretation of the fossils. lution of hominin locomotion. It is the model to
which we will compare the new fossils in order to The second hypothesis is the first of two that have
assess the trajectory of early hominin locomotion, received much broader support by data and by the
and is central to our understanding of early hominin paleoanthropological community. This position has
evolution. So, resolving the debate over its locomotor been articulated most clearly and extensively by
behavior, and its biology, is still a critical concern of Stern, Susman, and Jungers (summarized by Stern,
paleoanthropology. 2000), and states that A. afarensis individuals were
primarily terrestrial bipeds, but they also climbed
CURRENT HYPOTHESES OF trees (e.g., Senut, 1980; Berge and Ponge, 1983;
AUSTRALOPITHECUS AFARENSIS Jungers and Stern, 1983; Schmid, 1983; Stern and
LOCOMOTOR BEHAVIOR Susman, 1983, 1991; Tardieu, 1986a, b, 1999; Berge,
1984, 1991, 1994; Rose, 1984; Susman et al., 1984;
The first of three hypotheses suggests that A. Berge and Kazmierczak, 1986; Duncan et al., 1994;
afarensis individuals were palmigrade-plantigrade Hunt, 1994; Schmitt et al, 1996; Stern, 1999, 2000).
quadrupeds (Sarmiento, 1987, 1994, 1998). This These researchers based their conclusions on the
idea is based primarily on a suite of morphological mosaic of morphological features found in the A.
similarities between the hands and feet of A. afaren- afarensis skeleton (see McHenry, 1994; Stern, 2000).
sis and gorillas, in particular lowland gorillas, which They acknowledged the suite of features reflecting
Sarmiento (1987, 1994, 1998) argued are adapta- upright bipedal progression, but also emphasized
tions to weight transfer through the fore- and hind- numerous ape-like characters. They argued that
limbs during quadrupedal progression. For example, when reconstructing the probable positional behav-
Australopithecus and Gorilla share shorter fingers iors of A. afarensis, as for any fossil taxon, one must
and toes than typical for other great apes, a similar consider the total morphological pattern evident in a
morphology of the hamate-triquetral facet, a more skeleton (Le Gros Clark, 1955; Stern and Susman,
palmarly directed hamulus and pisiform, broad tib- 1991). From this perspective, all features of an or-
ialis posterior insertion, and large plantar aponeu- ganism are valuable and used, and if there are any
rosis (Sarmiento, 1994). primitive traits retained in the skeleton, they must
While these similarities might seem to support be there for a functional reason. Some researchers
this hypothesis, the overwhelming suite of skeletal have gone one step further, suggesting that A. afa-
modifications that enhance bipedal posture and lo- rensis exhibits a compromise morphology, and that
comotion seen in Australopithecus, including the si- these primitive traits would have affected the na-
nusoidal vertebral curvatures (Robinson, 1972; ture of bipedal progression in Australopithecus
Ward and Latimer, 1991; but see Sarmiento, 1998), (Stern and Susman, 1983; Jungers, 1982; Jungers
short pelvis with laterally-rotated iliac blades (Jo- and Stern, 1983; Rose, 1984, 1991; Susman et al.,
hanson et al., 1982a; Tague and Lovejoy, 1986; Love- 1984; Schmitt et al, 1996, 1999; Stern, 1999), result-
joy et al., 1999), broad sacrum (Robinson, 1972; ing in a bent-knee, bent-hip bipedal progression.
Leutenegger and Kelly, 1977), and femoral neck The third hypothesis has also received widespread
structure and condyle shape (Lovejoy et al., 1973; support. The most widely published proponents of
Johanson et al., 1982a), are not shared with gorillas, this idea are Latimer, Lovejoy, and Ohman, and the
and do not support the hypothesis of quadrupedal clearest articulation of their perspective can be
posture or locomotion in Australopithecus. In partic- found in Latimer (1991). These researchers also in-
ular, the valgus angle of the knee of hominids is an terpret the numerous derived features of the A. afa-
epigenetically labile trait (Tardieu and Trinkaus, rensis skeleton as clear evidence of selection for ha-
1994; Duren and Ward, 1995; Duren, 1999) and bitual terrestrial bipedality. They note that because
demonstrates that A. afarensis walked upright not A. afarensis had not only acquired adaptations for
quadrupedally. In a recent study of the development bipedality, it had, in the process, reduced its arbo-
of a valgus knee in humans in normal and nonam- real efficiency by sacrificing traits such as relatively
bulatory myelodysplastic children, Duren (1999) long forelimbs, fingers, and toes, and perhaps most
found that a bicondylar angle was the direct result of importantly, a grasping foot (Latimer and Lovejoy,
a habitual bipedal gait. It does not form in these 1989; Latimer, 1991). They cite the clear vector of
affected individuals who engage only in intermit- morphological change (defined as the magnitude
tent, or facultative, bipedality. The presence of a and direction of morphological character transfor-
valgus knee in Australopithecus demonstrates that mation throughout a lineage; Simpson, 1953) that
it was a habitual biped, falsifying the hypothesis of was towards anatomy that enhanced terrestrial
Sarmiento (1987, 1994, 1998). Many shared similar- bipedality and diminished arboreal competence
ities of early hominins and gorillas may be primi- (Latimer, 1991). Thus, the shift away from features
tive, and do not necessarily signify equivalent adap- enhancing arboreal ability must derive from a be-
tations to a particular shared locomotor repertoire havioral repertoire in which arboreality was not fa-
in these taxa. Alternately, they could be homopla- vored by selection (Latimer, 1991). Hence, arboreal-
sies evolved for different purposes in hominins and ity must have been relatively unimportant for
gorillas. Therefore, this hypothesis will not be dealt survival and reproduction in A. afarensis and its
with further here. immediate ancestors. They argue that if A. afarensis
individuals did climb trees, arboreal agility had lit- expense of arboreal function, most notably the loss
tle adaptive significance for them. Although at one of a divergent hallux, reduction in intermembral
point Lovejoy (1988) went one step further to add index, and shorter fingers and toes. These changes
that A. afarensis not only was not adapted to climb imply that agile movement in the trees was of lesser
trees, but could not have done so effectively without reproductive value than was bipedality for the an-
adverse consequences for their fitness, he later re- cestors of A. afarensis. This is not to say that arbo-
turned to the argument that that it simply is not reality was not also selectively valuable, but per-
possible to determine the fitness benefits of arbore- haps it was to a lesser degree. Diminished arboreal
ality in A. afarensis (Ohman et al., 1997). competence did not result in a selective disadvan-
In summary, these latter two hypotheses about tage to the immediate ancestors of A. afarensis,
early hominin locomotion are in complete accord however.
over the fact that the recent ancestors of A. afarensis In this case, the retention of features ordinarily
had undergone selection for terrestrial bipedal loco- associated with arboreal progression, such as fore-
motion. They differ substantially only over the rel- limbs longer relative to hindlimbs, or phalanges
ative importance of arboreality for A. afarensis. longer and more curved compared with those of hu-
REASONS FOR THE DEBATE mans, is inherently difficult to explain (see Gould
and Lewontin, 1979; Bock, 1980, Baum and Larson,
The first step necessary in unraveling the nature 1991; VanValkenburgh, 1994; Lauder, 1995, 1996).
of early hominin bipedality is to understand the Such traits could have been actively retained by
nature of the disagreements over interpretations of stabilizing selection because they continued to en-
A. afarensis locomotion. The debate is not due to a hance the survival and reproductive success of their
lack of fossil evidence, because A. afarensis is known bearers by enabling them to be more agile tree
from most skeletal elements. There are a few dis- climbers than they would otherwise be (adaptations;
agreements over interpretations of available fossil Gould and Vrba, 1982). Alternately, they may sim-
evidence (summarized in Stern, 2000), but the de- ply have been features that did not compromise ar-
bate has two more significant causes. First, re- boreality and were neither selected for nor against
searchers have different approaches to interpreting (nonaptations; Gould and Vrba, 1982). They may
anatomy, and in particular primitive retentions even have been in the process of being selected
(Latimer, 1991; Coffing, 1999). Second, and equally against (disaptations; Gould and Vrba, 1982). Be-
importantly, they are asking fundamentally differ- cause any of these three mechanisms can occur, and
ent questions of the data. undoubtedly does occur, these hypotheses are im-
One reason for the disagreement over Australo- possible to test without further information.
pithecus locomotion is a fundamental philosophical Latimer, Lovejoy, and Ohman argue that because
difference in the interpretation of primitive charac- we cannot readily test these hypotheses, we cannot
ters (Coffing, 1999). Derived signals in morphology consider the adaptive value of retained primitive
are relatively easy to interpret. The numerous de- traits. Stern, Susman, and Jungers, on the other
rived traits of Australopithecus have been shown by hand, argue that the stabilizing selection hypothesis
biomechanical analyses to be accommodations for is the only logical one to explain the maintenance of
weight-bearing and movement in upright bipedal the numerous primitive features of A. afarensis. Bi-
posture. These features, like sinusoidal vertebral ases towards one hypothesis can color researchers’
curvatures or an adducted hallux, are unambiguous, interpretations of the adaptive role of morphological
and are considered adaptations to habitual upright structures, and thus the biology and behavior of
posture and locomotion. Their unambiguous polar- extinct animals.
ity, coupled with their clear affect on function (in the The second, and equally important, reason for the
sense of Lauder, 1996: the use or action of pheno- disagreement over Australopithecus locomotion is
typic features), reveals their biological role (again as that these two sets of researchers are asking differ-
in Lauder, 1996: the role of phenotypic features in a ent questions. Latimer, Lovejoy, and Ohman are
specific environmental or ecological setting) for bi- interested in attempting to reconstruct the pattern
pedal progression (Weishampel, 1995). These char- of natural selection that produced A. afarensis: why
acters tell us that the ability to walk upright did A. afarensis evolve? They would argue that it
conferred significant fitness benefits on those indi- does not matter what actual activities individuals
viduals better designed to deal with the mechanical engaged in over the course of the day; the strength of
demands of terrestrial bipedality. selection on a particular trait that affects a behavior
The ape-like features of Australopithecus, on the is not proportional to the time the individual en-
other hand, are generally assumed to be primitive gages in that behavior. Individuals sit, sleep, and
retentions (lists in McHenry, 1994; Stern, 2000), and engage in many other activities that do not impose
many probably are. Interpreting why these primi- adaptively significant consequences on those indi-
tive features are retained in A. afarensis, or any viduals that do not possess morphologies particu-
taxon, is where perspectives diverge. Australopithe- larly suited to those activities. In other words, all
cus had undergone numerous modifications that activities do not have the same fitness effects with
served to enhance terrestrial bipedal function at the respect to the skeleton. They argue that we simply
cannot know, nor is it necessary to know, all of the next step is to identify specific hypotheses and cri-
behaviors in which the animals engaged. If we are teria for their potential falsification. To address the
interested in reconstructing adaptive history, then it question of selective history, we first must under-
is the vectors of morphological change (Simpson, stand the polarity of traits we are considering, and
1953) that will reflect vectors of selection acting on a the vectors of morphological change apparent in the
lineage, and provide the answers we seek (Latimer, early hominin skeleton. To answer either question,
1991). Stabilizing selection is harder to discriminate we need to better understand morphology and its
from lack of selection for primitive structures, influences. Not all traits provide similar information
Latimer (1991) argues, so we must restrict basing about fossil taxa (e.g., Cartmill, 1994; Churchill,
our hypotheses about selective pressures that 1996; Lieberman, 1997; Lovejoy et al., 1999, 2000).
shaped a lineage to evidence from directional change Some will tell us more about genetic change within
within that lineage. a species, and therefore the history of selection, and
Stern, Susman, and Jungers are asking a differ- some will tell us more about an individual’s behavior
ent question (Stern and Susman, 1983, 1991; Sus- over the course of its lifetime.
man et al., 1984; Susman and Stern, 1991; summa-
Hypotheses about adaptation
rized in Stern, 2000). They are attempting to infer
the actual behavioral repertoires of A. afarensis in- To infer the selective regime acting on a species
dividuals, and not the history of selection. These from morphology alone is notoriously difficult, and a
researchers note that individuals engage in varied substantial literature is devoted to this issue (e.g.,
locomotor activities over the course of days and life- Gans, 1966; Gould and Lewontin, 1979; Bock, 1980;
times. Their approach seeks to identify what types of Wake, 1982; Arnold, 1983; Mayr, 1983; Baum and
behaviors one might see A. afarensis engaged in if Larson, 1991; Leroi et al., 1994; Koehl, 1996; papers
one traveled back in time to observe them: what was and references in Thomason, 1995; Rose and
their locomotor repertoire? Stern (2000) chooses a Lauder, 1996). Without ecological data and data
quote from Duncan et al. (1994, p. 79) that summa- about which behaviors affect fitness in which ways,
rizes their philosophy: “understanding the overall we lack critical information that would enable us to
functional pattern (emphasis mine) of the organism actually test hypotheses about the selective regimes
requires an equal consideration of all its anatomical acting on A. afarensis (Baum and Larson, 1991;
features, regardless of whether they are apomor- Koehl, 1996; Larson and Losos, 1996). Instead, we
phies, plesiomorphies or homoplasies. This view- must rely on phylogeny, biomechanical modeling,
point serves to frame the fossils as once fully func- and comparative morphology to support or refute
tional living organism.” Stern, Susman, and Jungers hypotheses about selective pressures as best we can.
argue that this approach is indeed important, be- To construct hypotheses about the selective re-
cause in order to understand our ancestors, we need gime that shaped a taxon, one must first identify the
to be able to reconstruct their behavior. character transformations that occurred in that lin-
These two approaches are different, and comple- eage (Felsenstein, 1985; Brooks and MacLennan,
mentary rather than mutually exclusive. Thus, the 1991; Harvey and Pagel, 1991; Kay and Covert,
apparent debate as it has been framed is not a true 1984; Lauder, 1995, 1996; Weishampel, 1995; Wit-
debate. It is important to keep in mind the distinc- mer, 1995; Larson and Losos, 1996; Begun et al.,
tion between reconstructing behaviors from recon- 1997a,b). This depends on having a reliable phylog-
structing evolutionary pressures. Neither approach eny from which one can reconstruct ancestral char-
to understanding Australopithecus is better or worse acter states. In the case of Australopithecus, molec-
than the other. They are intrinsically different, how- ular studies have produced robust hypotheses about
ever. They address the data differently, and rely on extant hominoid relationships (see Ruvolo, 1997).
different characters for different reasons. They This may not be enough to reconstruct the character
should not be contrasted as opposite sides of a single states of the last common ancestor of apes and homi-
argument. Both questions are worth pursuing. We nins, however. The burgeoning fossil record of Mio-
need to understand the types of animals early homi- cene and Pliocene apes, including hominins, slowly
nins were, as well as the history of selection that continues to add more data with which to develop
shaped them. It is time to recognize the differences and test phylogenetic hypotheses among living and
in these approaches, note their inherent limitations, fossil taxa. Because these fossil taxa do not resemble
and proceed. extant species in all features, they stand to alter the
EMPIRICAL FRAMEWORKS balance of parsimony for traits, and so could affect
our interpretations of the primitive conditions from
To move forward in our understanding of Austra- which Australopithecus or other early hominins
lopithecus locomotor behavior, we need to focus our evolved. Continual attention to phylogenetic analy-
approach to interpreting the fossils. The first step is ses of hominoids will be critical to our ability to
to be explicit about what questions we are asking. reconstruct character transformations that pro-
Do we want to reconstruct the history of natural duced Australopithecus and other early hominins.
selection shaping the hominin lineage(s), or the lo- While drift and other random forces may have
comotor/behavioral repertoires of fossil taxa? The lasting impacts on species over time (see Nitecki,
1990), the only evolutionary force that can produce ing selection. Even if a trait was neutral with re-
long-term directional change is selection, particu- spect to selection, a trait could be pleiotropically or
larly when there is a broad suite of features that all structurally linked to other traits that were under
enhance the same function, e.g., bipedality in Aus- selective influence. Its maintenance could reflect
tralopithecus. Therefore, it is reasonable to infer lack of selection to change a developmental cascade
that when long-term directional change is observed influencing other structures that are themselves be-
within a lineage, especially in numerous characters ing maintained by stabilizing selection (discussions
or character complexes, that selection for a behavior in Maynard Smith et al., 1985; Churchill, 1996).
influenced by the observed morphology was the A final hypothesis for the retention of primitive
cause. traits could be that they were actively being selected
Biomechanical modeling and comparative studies against, but that selection had not had sufficient
can help reveal the biological roles of the newly time to reduce or eliminate them. This hypothesis of
transformed structures by determining which func- disaptation would require that the trait would di-
tion or functions they enhance (Baum and Larson, minish or change over time, and not persist unal-
1991; Weishampel, 1995; Lauder, 1995, 1996). Cou- tered.
pling phylogenetic data with biomechanical data al- A similar conundrum to the issue of arboreality in
lows paleontologists to form reasonable hypotheses A. afarensis lies in the interpretation of the rudi-
about the behaviors on which selection acted. If phy- mentary forelimbs in Tyrannosaurus rex (Carpenter
logenetic analysis determines that a structure is and Smith, 2001). Here also is a case where primi-
apomorphic, and mechanical analysis determines tive features, in this case forelimbs, have been re-
the function it enhances, we can hypothesize that tained but altered in the light of a strong directional
selection for that function produced the structure signal towards a new behavior, terrestrial bipedal-
(Weishampel. 1995). Comparative morphological ity. So, are these tiny forelimbs still present because
and behavioral studies can be used to support hy- they serve an adaptive function for some altered
potheses of adaptation when similarly constructed task, or are they retained for no reason? Some of the
modern animals are known to share a similar func- debate over their function takes the form of logical
tion. In the case of A. afarensis, there are numerous arguments, which are not necessarily empirical (Os-
derived modifications of their skeletons that en- born, 1906; Newman, 1970; Paul, 1988). The most
hance terrestrial bipedal progression and resemble recent contribution uses forelimb bone robusticity
modern hominoid bipeds. Thus, we can hypothesize and inferred muscle size and strength to argue that
that these characters were shaped by selection for these are not useless, vestigial structures (Carpen-
bipedal locomotor abilities. ter and Smith, 2001). Because both of these features
Testing hypotheses about the retention of primi- are influenced by behavior, this evidence suggests
tive traits is more difficult (e.g., Frumhoff and that the forelimbs were still used for some purpose,
Reeve, 1994). When a primitive trait remains un- which Carpenter and Smith (2001) hypothesize was
modified in a taxon from the ancestral form, the null manipulating food items during oral processing.
hypothesis is that it is selectively neutral, termed a This case is still different from that in A. afarensis,
secondary nonaptation (Lauder, 1996). To falsify the however, because A. afarensis had not lost the abil-
null hypothesis, one must be able to show that sta- ity to use their primitive ape-like traits for their
bilizing selection or negative selection was at work. original function. It is, however, a useful example to
To demonstrate stabilizing selection for a primitive explore how hypotheses about the functional signif-
trait, one would need to show that the primitive icance of primitive traits, either adaptive and/or be-
structure compromised a derived function. In the havioral, can be tested.
case of Australopithecus, this would be whether its Unlike the Tyrannosaurus example, in which the
primitive traits compromised bipedality. question was if the structure was functional at all or
Other lines of evidence might be invoked as merely vestigial, a more relevant example is the
weaker support for the hypothesis of stabilizing se- hindlimbs of the primitive whale Ambulocetus
lection. If a trait was retained in its unmodified form (Thewissen et al., 1994). The retention of functional
for a substantial period of time (stasis), it is possible, hindlimbs in this taxon indicates that it could am-
but not certain, that stabilizing selection was in- bulate terrestrially, although there was a clear di-
volved. If one could demonstrate that an animal rectional signal towards an aquatic lifestyle. The
actually engaged in behaviors for which the primi- authors propose that the hindlimbs were propulsive
tive traits had been adaptations, it might suggest in the water and on the land. The vector of morpho-
continued adaptive value of these traits, but again logical change clearly was towards improving swim-
this would not be definitive. Even if these latter two ming ability at the expense of terrestriality. When
criteria (stasis or behavior) were met, they would Ambulocetus was terrestrial, it would have been rel-
still not falsify the null hypothesis of nonaptation. atively awkward in its movements. Knowing that it
They merely would be suggestive. If a trait was could have moved about on land, and even that it
selectively neutral, variation should increase over may have done so, it is still difficult to assess the
time (e.g., Tague, 1997, 2002a). However, the lack of adaptive significance of terrestriality in these early
increased variability still might not signal stabiliz- whales. Again, here the fossil record reveals the

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 grazers of abrasive C4 grasses. However, microwear
the pattern of selection that produced this change and isotope data suggest that they had a range of
relies on scientific inference. diets from browsing to grazing on many types of C3
We also need to be careful not to assume immedi- and C4 plants. Some species (particularly Dinohip-
ately that because Australopithecus did not look ex- pus mexicanus and Astrohippus stockii) were almost
actly like humans that its behavior was necessarily exclusively browsers. Hypsodonty appears to have
different. The retention of primitive traits does not been retained, perhaps because of some sort of phy-
always mean that these traits were maintained for logenetic and/or developmental constraint, although
their original function. Examples of discrepancies in behavior had changed.
form-function relationships between extant and fos- Another example comes from the primate litera-
sil taxa can and have been demonstrated between ture. Kay and Ungar (1997) showed that although
tooth morphology and diet, for which evidence of Miocene apes had a similar range of molar shearing
genetically based morphology (tooth form) can be crest lengths as do roughly the same taxonomic di-
compared to evidence of behavior (microwear and versity of extant species, the molars of all early
bone isotope analysis). One example of this phenom- Miocene taxa were all more bunodont than those of
enon was found in the teeth of late Miocene/early extant apes (Fig. 1). These data seem to suggest that
Pliocene horses from Florida (MacFadden et al., no Miocene apes were as folivorous as the most
1999). All six species examined in this study re- folivorous extant apes, i.e., gorillas and siamangs.
tained inherited high-crowned molars, and based on This may be incorrect, as Kay and Ungar (1997)
tooth morphology would have been interpreted as argued using microwear data. Their microwear
analyses showed that, in fact, the Miocene taxa were crowear, the pits and scratches on teeth caused by
eating the same range of diets seen in extant apes, diet. Given a constant pattern of enamel microstruc-
and that even species such as Rangwapithecus, ture and fracture behavior, which appears to be the
which had teeth with gross morphology most like case for all hominoids, microwear reveals individual
those of modern frugivores, were eating as many activity, but not adaptive history (Teaford, 1988,
leaves as do modern folivores. In effect, tooth mor- 1994). In contrast, because tooth shape appears to
phology improved over time. be conservative within taxa, it is generally assumed
This may well have happened in the evolution of to be tightly genetically controlled, and not influ-
hominin, and hominoid, postcranial anatomy, and it enced by an individual’s diet (although fetal envi-
may be possible to uncover the extent to which it ronment and nutrition may be involved in tooth
may have occurred by comparing traits with greater formation, diet appears not to be an influence). Vari-
or less epigenetic variability resulting from individ- ations in molar shearing crest length among taxa,
ual behaviors. It underscores the difficulty of inter- for example, are thus thought to reflect natural se-
preting actual behaviors in fossil taxa. lection on crest length in response to diet (Kay and
Hypotheses about behavior Hiiemae, 1974; Kay, 1975; Rosenberger and Kinzey,
1976; Strait, 1993a, b; Teaford, 2000). Tooth shape
On a practical level, precise interpretation of loco- and features such as molar shearing crest length
motor repertoires may exceed the limit of resolution reflect a history of selection, whereas microwear re-
possible in the fossil record. For example, humans in flects behavior.
many forager groups like the Yanamamo (Chagnon, Unfortunately, postcranial anatomy has few, if
1997) and Achuar climb trees for fruit and other food any, such dichotomies. Examples of epigenetically
resources (Descola, 1996a,b). This behavior is not plastic traits are physeal plate angles (Tardieu and
reflected in genetically determined skeletal mor- Trinkaus, 1994; Duren, 1999) and diaphyseal cross-
phology, because anatomical variation that im- sectional form (summarized in Martin et al., 1998;
proves arboreal abilities apparently has not affected Ruff, 2000), and may also include long bone torsion
their fitness. We would not be able to “see” the (Martin and Saller, 1959; King et al., 1969; Sar-
arboreality in their skeletons, just as we cannot miento, 1985; Pieper, 1988) and perhaps even pha-
“see” behaviors such as lying down or sitting, be- langeal curvature (Richmond, 1998) or aspects of
cause an individual’s anatomy does not affect his joint conformation (Frost, 1979, 1994; Hamrick,
fitness by allowing him to be more or less effective at 1999; but see Lieberman and Pearson, 2001). By
these behaviors (Latimer, 1991). There is no selec- carefully studying the influences of activity on bone
tive disadvantage of having anatomy that is poorly form, either directly or via soft tissues, we will be
designed for such tasks. This makes interpreting better able to use morphological information reliably
actual behaviors in extinct species particularly to reconstruct behavior. By identifying the develop-
tricky. It may be possible at some level, but will mental plasticity of morphology, we are better
always remain unsatisfying at another. If A. afaren- armed to reconstruct the behavioral repertoires of
sis climbed trees, we have to be clever enough to find fossils, and to avoid misinterpreting characters
ways to read this in their morphology, potentially when constructing phylogenies with morphological
using ontogenetically labile characters that can be data.
influenced by individual behaviors over the course of
a lifetime. Still, it is worth the attempt, so that we REEXAMINATION OF THE FOSSIL EVIDENCE
can better understand what our extinct relatives USING THIS FRAMEWORK
were like.
Armed with a more explicit identification of the
The simple presence of primitive features in the A.
questions we are asking about Australopithecus, we
afarensis skeleton is not enough to identify the
can begin to reevaluate the fossil record for early
adaptive value of tree climbing. For example, a fu-
hominin locomotion using this empirical framework.
ture paleoanthropologist studying skeletons of to-
For all phases of this process, it is important to
day’s humans could argue that because we retained
elucidate the genetic and ontogenetic influences on
a grasping hand and mobile shoulder joint, features
that evolved for an arboreal lifestyle, modern hu-
mans are partly arboreal. None of us, however,
Character polarities and vectors of
would argue that these traits were maintained by
morphological change in early hominins
selection on humans primarily for the ability to
climb trees well. Instead, these traits primarily rep- Reconstructing character transformations within
resent exaptations for manipulative or throwing hominoid lineages is notoriously difficult (Larson,
abilities, although they also are used in climbing 1998; Sarmiento, 1998; Begun, 1999; Richmond et
rocks or trees. al., 2001). Despite studies arguing that postcranial
Behavior of an extinct animal can be examined by data are more informative about phylogeny than are
considering morphological features that are shaped craniodental data (Collard and Wood, 2000), it is not
by its activity pattern. One of the best examples of the case that we can assume hominins evolved from
an environmentally determined trait is dental mi- an ancestor that was similar to extant great apes in
every aspect of its postcranial anatomy. Recent at- ing them to reconstruct character transformation
tention to the amount of apparent homoplasy in the through hominoids can we come close to uncovering
hominin skeleton (e.g., Larson, 1996, 1988; Begun et actual patterns of change in hominoid evolution. By
al., 1997a, b; Rose, 1997; Ward CV, 1997; Lieber- incorporating Miocene ape fossil data into our phylo-
man, 1999; Coffing and McHenry, 2000; Collard and genetic schemes, we may alter the balance of parsi-
Wood, 2000; MacLatchy et al., 2000) highlights our mony about any number of characteristics (e.g. Begun,
need to remain cautious in making polarity deter- 1994; Begun et al., 1997a; Rose, 1997; Ward CV, 1997).
minations, especially based on extant hominoid data Determining the phylogenetic relations among fossil
alone. Elucidating the genetic and ontogenetic influ- apes is problematic, of course. Furthermore, we can
ences on morphology will aid in the understanding never hope to recover the diversity of hominoid species
of its phylogenetic signals. Until we better under- that must have existed. Nonetheless, without consid-
stand these effects, we can continue to invoke par- ering what we do know and making careful hypotheses
simony arguments if we do cautiously, understand- about the relationships we have identified so far, we
ing their inherent limitations. We can be most neglect vital information about the pattern of evolu-
effective only by including all available data in con- tionary history that produced living hominoids. This
structing the phylogenies upon which we base our information may alter our perceptions of which homi-
polarity determinations. nin features are, in fact, derived, and which are prim-
Character selection determines our ability to itive.
make accurate phylogenetic hypotheses. This re- A recently published phylogeny of hominoids
quires careful choices of features, and knowledge based on 240 characters of craniofacial, dental, and
about the individual variability, phenotypic plastic- postcranial skeletons is the most robust phylogeny
ity, and heritability of traits (e.g., Cartmill, 1994; of these taxa constructed to date (Fig. 2) (Begun et
Weishampel, 1995; Lieberman, 1997, 1999), as well al., 1997a). Using this as a baseline, we can examine
about genetic and ontogenetic links among them. As the likely polarities of the ape-like traits of A. afa-
the determinants of adult form become clearer, and rensis. Not all features are known from the euhomi-
we can identify behavioral or functional influences noid (the clade including living hominoids; see Fig.
on morphology, we can use these inferences to make 2) fossil record, such as proportions within and
hypotheses about the behaviors of A. afarensis and among pedal digits, or overall foot length. Still, the
its ancestors, allowing us to reconstruct the history approach will allow us to test hypotheses of adapta-
of selection that led to bipedality (Richmond and tion, stasis, and disaptation for most characters.
Strait, 2000; Richmond et al., 2001 and references One impact of fossil data on interpreting charac-
therein). Functional anatomy is not unrelated to ter transformations leading to hominins has been in
phylogenetic reconstruction, as it both informs char- the realization that extant great apes’ postcranial
acter selection and provides a venue in which to test anatomy may not all be homologous. Sivapithecus is
phylogenetic hypotheses (Brooks and MacLennan, widely considered to be the sister taxon of Pongo
1991; Harvey and Pagel, 1991; Weishampel, 1995; (review in Ward S, 1997). Because humeral torsion
Witmer, 1995; Begun et al., 1997a; Ward et al., is presumed to reflect shoulder joint orientation
1997). Functional and phylogenetic interpretations (Evans and Krahl, 1945; Le Gros Clark and Thomas,
are codependent. Thus, our phylogenetic reconstruc- 1951; Martin and Saller, 1959; Napier and Davis,
tions are critical to reconstructing the vectors of 1959; Larson, 1996, 1998; Pilbeam et al., 1990;
change. Churchill, 1996), and therefore reorganization of
Based on extant hominoid taxa alone, our percep- torso structure (Benton, 1965, 1976; Ward, 1993;
tion of character transformation would be relatively Ward et al., 1993; Churchill, 1996; but see Chan,
straightforward. All four great ape species share a 1997), this character has particular importance (al-
suite of morphologies that enhance their abilities to though it can be epigenetically modified by behavior
engage in vertical climbing and below-branch arbo- pattern; Martin and Saller, 1959; King et al., 1969;
real activities, given their relatively large body Sarmiento, 1985; Pieper, 1998). The large Sivapithe-
sizes. These include a strongly grasping hallux and cus parvada humerus from Sethi Nagri (GSP 30754)
pollex, a restructured torso involving laterally facing has less torsion than any extant hominoid, instead
shoulder joints, a high intermembral index, long, more closely resembling pronograde quadrupeds
curved phalanges, strong manual and pedal grasps, (Larson, 1996, 1998; Pilbeam et al., 1990; Madar,
short lumbar vertebral columns, and craniocaudally 1994; Ward S, 1997).2 Furthermore, the Sivapithe-
elongate pelves. Modern great apes differ in compar- cus postcrania also reveal that members of this ge-
atively minor ways. With no further information, nus had less well-developed halluces than do extant
it would seem clear that these shared features orangutans or African apes, and shorter, less curved
were indisputably homologous, and that hominins
evolved from an ancestor that was postcranially
much like extant great apes. 2
Moyà-Solà and Köhler (1996) reconstructed the smaller Sivapithe-
However, extant hominoids are relics from an ear- cus humerus from a cast, and inferred a different functional pattern.
lier and more diverse age. The vast majority of homi- If their conclusion is supported by further analyses, this might indi-
noid taxa that once existed are extinct. Only by includ- cate locomotor diversity within the genus.

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

phalanges (Rose, 1986, 1997; Spoor et al., 1991; al., 2000), suggesting a similar adaptive response in
Begun, 1993). Their inferred torso structure, which closely related organisms subjected to similar selec-
reflects a ventrally oriented scapular glenoid fossae tive pressures (e.g., Jolly, 2001). The likelihood of
and an emphasis on flexion-extension abilities of the independent acquisition of the Pongo and Sivapithe-
proximal forelimb at the expense of abduction-ad- cus craniofacial similarities is less certain at this
duction movements, and appendicular characters point (Ward S, 1997).
perhaps indicating less well-developed manual and Hominins also share features with fossil “basal”
pedal grasping ability, are more like those of basal hominoids (Begun and Kordos, 1997; Begun et al.,
hominoids such as Proconsul (summarized in Ward 1997a,b) such as Sivapithecus, Proconsul, and/or
S, 1997). Equatorius, and with Hylobates, that are not found
These Sivapithecus postcranial fossils imply that among extant great apes, such as shorter pelves
either Pongo is convergent upon African apes in
with longer lumbar vertebral columns, less curved
many of its more specialized climbing features, or
that the many craniofacial similarities of Pongo and forelimb bones, longer thumbs, shorter medial rays
Sivapithecus are homoplasies (Pilbeam et al., 1990; of the hand and foot, and less humeral torsion (e.g.,
Ward S, 1997). Either of these hypotheses is plausi- Larson, 1996, 1998; Rose, 1997; Ward CV, 1997;
ble, but they are mutually exclusive. The possibility MacLatchy et al., 2000). Foot length is not known
of Asian and African great apes sharing postcranial from the fossil record after Proconsul, whose feet
homoplasies linked with below-branch arboreality is were not as long as those of extant apes (Walker and
not unreasonable, given the apparent independent Teaford, 1988). Either hominins have reverted to the
acquisition of some of these morphologies in Moro- primitive condition in these features, or extant apes
topithecus and atelines (Walker and Rose, 1968; are homoplastic in these ways. Either scenario in-
Ward CV, 1993, 1997; Sanders and Bodenbender, volves substantial homoplasy, making polarity de-
1994; MacLatchy, 1996; Rose, 1997; MacLatchy et terminations among hominoids difficult.
The likely Asian-African ape homoplasies open 1996), Orrorin (Senut et al., 2001), and Ardipithecus
the possibility that chimps and gorillas may also be (Haile-Selassie, 2001), and in extant apes, although
homoplastic in some features. This hypothesis is less so in early hominoid taxa (Begun, 1994; Rose,
supported by some researchers studying kinematic 1997). Australopithecus appears to have had re-
and anatomical correlates of knuckle-walking in duced manual and pedal phalanges that were rela-
chimps and gorillas (Inouye, 1994; Dainton and Ma- tively shorter than in any primate except Homo
cho, 1999). If so, some of these hominin characters (Bush et al., 1982; White, 1994).3 The hamate ham-
may be primitive, which would indicate less change ulus is only somewhat distally directed, intermedi-
from the last common ancestor than we now sup- ate between extant apes and humans (Sarmiento,
pose. Recently, however, strong arguments were 1994, 1998; Ward et al., 1999b). The large hamulus
made in favor of the hypothesis that the last com- appears to be found only in African apes and homi-
mon ancestor was a knuckle-walker, and that Afri- nins, and is not present in Sivapithecus (Spoor et al.,
can ape postcranial similarities are indeed homolo- 1991) or Proconsul (Beard et al., 1986). Hamulus
gous (Richmond et al., 2001). This perspective is the form likely reflects morphology of the carpal tunnel
most widely accepted at present. Further research rather than flexor carpi ulnaris function, as previ-
into the function and evolution of the forelimb is ously suggested (Sarmiento, 1998; Ward et al.,
needed to continue to test these competing hypoth- 1999b). However, the pisohamate ligament inserts
eses. not on the distal end of the hamulus, but at its base,
Most A. afarensis traits interpreted as primitive, at least in chimpanzees and humans (personal ob-
based on comparison with extant taxa (McHenry, servation). Thus, hamulus size and orientation ap-
1994; Stern, 2000), still appear to be primitive even pear not to reflect the flexor carpi ulnaris muscle or
when the fossil evidence is considered. A long pisi-
pisohamate ligament, but the palmar carpal liga-
form, dorsoplantarly narrow navicular, and meta-
ment (flexor retinaculum), which forms the roof of
tarsals lacking expanded dorsal margins of their
the carpal tunnel. It is certainly possible that carpal
head are known for Oreopithecus (Sarmiento, 1987)
tunnel length is related to overall hand length, and
and extant apes. Australopithecus lacks the ex-
if so, hamulus distal projection may be related to
panded vertebral bodies of humans, resembling all
taxa for which there are data (e.g., McHenry, 1992): hand length at least at some level. A. afarensis ap-
Proconsul (Napier and Davis, 1959; Walker and pears to have reduced the proximodistal length of its
Pickford, 1983; Walker and Teaford, 1988; Ward et carpal tunnel relative to African apes.
al., 1993), Nacholapithecus (Rose et al., 1996a,b; The high intermembral index (calculated as (hu-
Nakatsukasa et al., 1998, 2000), Equatorius (Le merus ⫹ radius/femur ⫹ tibia) * 100) of African apes
Gros Clark and Leakey, 1951), Morotopithecus appears to have been present in at least Oreopithe-
(Walker and Rose, 1968; Gebo et al., 1997; Mac- cus (Hürzeler, 1960; Moyà-Solà and Köhler, 1996)
Latchy et al., 2000), Oreopithecus (Harrison, 1986; and Dryopithecus (Moyà-Solà and Köhler, 1996), al-
Sarmiento, 1987), Dryopithecus (Moyà-Solà and though not in Proconsul (Walker and Pickford, 1983;
Köhler, 1996), and extant primates. Within the Walker and Teaford, 1988). Although Dryopithecus
hand, a pronounced third metacarpal styloid pro- was interpreted to have an intermembral index
cess, found only in Homo and some gorillas, is ab- higher than that of African apes and only like oran-
sent in Proconsul (Napier and Davis, 1959) and gutans among extant species (Moyà-Solà and
Oreopithecus (Moyà-Solà et al., 1999). Also, the first Köhler, 1996), it may not have been as extreme, as
metacarpal base highly is concavoconvex in Procon- these data were based on extensive segment length
sul (personal observation), Sivapithecus (Spoor et reconstructions. Direct comparison of the reported
al., 1991), Oreopithecus (Moyà-Solà et al., 1999), and ulna to femur lengths published with the fossil an-
extant apes. Small apical tufts are found on the nouncement (Moyà-Solà and Köhler, 1996) is 102,
distal phalanges of Afropithecus (Leakey et al., close to the African ape range (chimpanzees, 87–97;
1988), Proconsul (Napier and Davis, 1959; Begun, gorillas, 91–101), and considerably less than that of
1994), Nacholapithecus (Nakatsukasa et al., 1998), orangutans (128 –130). Oreopithecus, on the other
Oreopithecus (Moyà-Solà et al., 1999), Dryopithecus hand, is intermediate between extant African and
(Moyà-Solà and Köhler, 1996), and extant primates. Asian apes, with an ulna/femur ratio of 111. Austra-
The mediolaterally broad knee joint, typical of ex- lopithecus had an ulna (length estimate based on
tant apes and seen to a lesser extant in A. afarensis Drapeau, 2001) to femur length of about 80, showing
(Tardieu, 1979, 1981), is also known for Proconsul an apparent reduction in forelimb to hindlimb pro-
(Walker and Pickford, 1983) and Oreopithecus (Har- portions. This is evident in comparisons of humeral
rison, 1986; Sarmiento, 1987). to femoral proportions as well (Jungers, 1982, 1994;
Many primitive traits, however, are derived to- Wolpoff, 1983; White et al., 1993; White, 1994).
ward a human-like condition from the ape-like one.
Long, curved phalanges with pronounced flexor
ridges are found in Oreopithecus (Harrison, 1986; 3
In this paper, the term Homo is used to include Homo erectus/
Sarmiento, 1987; Moyà-Solà et al., 1999), Dryopithe- ergaster and more recent members of the genus Homo only, following
cus (Begun, 1992, 1993; Moyà-Solà and Köhler, the grade-based approach of Wood and Collard (1999).
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
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
hallucal abduction in any Australopithecus, it is dipithecus has also been described as a biped, based
highly unlikely that the rounded head of the first on a short basicranium in A. ramidus ramidus
metatarsal reflects opposability, but whether it (White et al., 1994) as in Sahelanthropus (Brunet et
somehow reflects arboreality is unspecified and un- al., 2002), and on a proximal phalanx of A. ramidus
known. kedabba that resembles those at Hadar (Haile-
Taken together, though, these indicators of a Selassie, 2001). A. r. kedabba also appears to have
somewhat primitive muscle configuration in Austra- had a curved ulna, but this is found in hominin
lopithecus suggest that these early hominins were ulnas from the Omo River Valley (Omo L40-19) and
not fully modern in their muscular anatomy. This is Olduvai Gorge (OH 36). The published forearm re-
an important point, because when muscles contract mains of A. r. ramidus appear more like those of A.
to respond to ground reaction forces or produce afarensis than African apes, but few details have
movement, they generate strain within bones that been published so far.
can trigger modeling responses during growth and So, in summary, most features of A. afarensis that
remodeling after skeletal maturity (review and dis- are generally interpreted to be primitive probably
cussion in Martin et al., 1998; Carter and Beaupré, are, although the prevalence of homoplasy among
2001). This means that some bony differences be- hominoids should suggest caution in making this
tween Australopithecus and humans could be re- assumption. The likely homoplasies between Asian
lated to one of two factors, or both. Either these and African apes raise the possibility that African
hominins were behaving differently, or they were apes may be convergent upon one another in ways
behaving in the same way but with slightly different other than forelimb length, making some apparently
muscle vectors due to the primitive muscle arrange- derived hominin features possible homoplasies, such
ment. The latter situation could produce a slightly as relatively short forelimbs, short pelves, 5– 6 lum-
different pattern of bone strain, influencing traits bar vertebrae, and thumb-finger proportions. This
such as the geometry of the acetabulum, proximal could be true even if the last common ancestor of
femoral shaft, patellar groove, or hallucal tarso- African apes and humans was a knuckle-walker.
metatarsal joint shape. Indeed, Berge (1991) hy- Some features that appeared to be derived in A.
pothesized that A. afarensis only could have moved afarensis, such as the short metacarpals or forelimb
bipedally efficiently if it had a more ape-like ar- proportions, appear to be primitive, with extant apes
rangement of the hip musculature due to its slightly often displaying a derived condition. Extant apes
different bone structure. Although these ideas have cannot be assumed to represent the primitive condi-
not been tested, they represent a plausible alternate tion, illustrated by the autapomorphic, relatively
hypothesis that should be considered when evaluat- long metacarpals of Pan. Ignoring the Miocene fossil
ing skeletal differences among hominins. record obscures potentially critical information, and
Another feature in which A. afarensis has been new fossils will certainly help answer the questions.
considered significantly different from humans is in
the anteroposteriorly compressed sacral ala. How- Do the derived traits of A. afarensis
ever, given the mediolaterally extensive and antero- reflect bipedality?
posteriorly compressed nature of the A. afarensis
Because there is such an extensive literature on
pelvis, and the broadly flaring blades, this feature
this subject, I will not review it here. Derived trait
may simply reflect iliac form and may not be a rel-
lists and discussions of their significance can be
evant variable itself (see Lovejoy et al., 2000).
found in McHenry (1994) and Stern (2000), and are
A final line of evidence we can use to assess char-
reviewed in Aiello and Dean (1990). The skull, ver-
acter polarities involves the few data now available
tebral column, pelvis, and entire lower limb all re-
for the earliest putative hominins Sahelanthropus,
flect clear and unambiguous characters recognized
Orrorin, and Ardipithecus. All three genera have
as adaptations for upright, bipedal progression by
been described as probable bipeds, but the nature of
numerous mechanical analyses. They are all traits
this bipedality and their morphological similarity to
shared at least to some extent with humans, the
later hominins are still unknown or undescribed.
only bipedal hominoids. These changes and their
Sahelanthropus is known only from a cranium. Be-
similarities to modern humans are far more exten-
cause it has a short basicranium with the basion
sive than the differences due to retained primitive
intersected by the bicarotid cord, like other homi-
characters. This suggests that they were indeed ad-
nins, its discoverers tentatively suggest it was up-
aptations shaped by natural selection for bipedal
right, barring further evidence (Brunet et al., 2002).
posture and locomotion (Weishampel, 1995; Lauder,
A nearly complete femur is known for Orrorin,
which its discoverers say displays bipedal features
(Senut et al., 2001). None of the characters they
Did primitive traits compromise bipedality?
mention in their article, however, are exclusively
found in bipeds. It could be that when the internal To test whether or not primitive traits were re-
contours of the femoral neck are revealed, and when tained by stabilizing selection, we first need to con-
proximal to middle shaft dimensions are compared, sider whether they compromised the derived func-
the data will be sufficient to make a judgment. Ar- tion. In other words, we need to test whether the
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 Fig. 4. Distance between superior zygapophyseal facet joints
in caudal eight vertebrae of Homo sapiens with 5 and 6 lumbar
capable bipeds, or if they differed from us, exactly vertebrae, respectively, Pan troglodytes, Australopithecus africa-
how. If Australopithecus could not walk as fast, far, nus STS 14, and A. afarensis AL 288-1. All hominins have in-
or well as do humans, and this was because of the creasing lumbar interfacet distances throughout lumbar skele-
retention of traits that enhanced arboreality, then ton, but chimpanzees do not. This uniquely hominin trait reflects
this would support the hypothesis that stabilizing presence of a lumbar lordosis, as it allows zygapophyses to slide
past each other when spine is extended, permitting lordotic pos-
selection had acted to maintain at some level of ture (Latimer and Ward, 1993). Data from Ward and Latimer
arboreal competence. (1991). Line drawing by Luba Gutz, from Latimer and Ward
Abitbol (1995) argued that A. afarensis had a low (1993).
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° unlikely from a kinematic perspective, however, as
for humans, which I think is a likely underestimate demonstrated by Crompton et al. (1998) and Kramer
of variability, as I have a human skeleton with an and Eck (2000) using modeling. They demonstrated
angle of 67°). He argues that this would necessitate that the lower limb length and conformation of AL
having their sacrum and pelvis in a more vertical 288-1 would not have produced a less energetically
position than is typical for humans. This difference efficient gait than in modern humans at walking
in sacral angle could be accommodated by the less speeds, and Kramer and Eck (2000) even suggested
anteriorly curved morphology of the sacrum, how- they might have even been more efficient. Kramer
ever, certainly when combined with a lumbar lordo- and Eck (2000) argued that the preferred transition
sis, allowing the lumbosacral joint to lie in the same speed from walking to running would have been
plane as that of humans despite the different sacral lower in A. afarensis than in humans. They went on
angle. A. afarensis certainly had a significant lum- to suggest that this would have affected distance of
bar lordosis, as it has a wide lumbar interfacet dis- travel or day range, although there appears to be no
tance between the presumed second lumbar and reason to assume any effect on day range based on
first sacral vertebrae (Fig. 4). Increasing interfacet their analysis.
distances allow the articular processes to imbricate, Ruff (1998) and Rak (1991) both argued that the
minimizing the probability of developing spondylol- anatomy of AL 288-1 could only be explained if A.
ysis and spondylolisthesis (Latimer and Ward, afarensis walked with greater pelvic movements
1993). Because significant posterior wedging of the than do modern humans, although neither of them
vertebral bodies occurs only in the last four lumbar proposes a bent-hip-and-knee gait. AL 288-1 has
vertebrae (Fig. 4) (Latimer and Ward, 1993), the fact femoral head dimensions expected for a hominin of
the second lumbar vertebra preserved in AL 288-1 is her size (McHenry, 1991; Ruff, 1998), and her fem-
not wedged is irrelevant. A lumbar lordosis indicates oral diaphysis is even stronger. However, because of
habitual upright posture. It even occurs slightly, this, coupled with her longer femoral neck, Ruff
although to a much lesser degree, in modern nonhu- (1998) suggested that A. afarensis pelvic movements
man primates trained to walk bipedally (Nakat- during gait would have had to be greater because of
sukasa, 1991). greater predicted hip and femoral strains. Because
Some researchers have proposed that A. afarensis his analysis of mediolateral bone strength was made
gait was kinematically distinct from that of humans, in relation to anteroposterior strength, the fact that
and that they walked with their hips and knees in a A. afarensis seems to have had proportionally stron-
more flexed posture (Susman et al., 1984; Preuschoft ger bones throughout its skeleton (Ruff, 1998; Coff-
and Witte, 1991; Stern, 1999). A bent-knee gait is ing, 1998) could confound his comparison. It is also

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 as do modern humans (Fig. 5). Even though the
bicondylar angle in this situation. Still, Ruff (1998) degree of femoral condylar flattening may not be as
did not argue for a bent hip posture. Rak (1991) also extensive as in most adult modern humans, their
posited greater pelvic movements, although in pelvic shape is fully human-like and resembles that of
rotation rather than lateral elevation. Neither of modern 10 –12-year-old humans (Tardieu, 1998).
these situations was modeled by Crompton et al. This morphology serves to increase tibiofemoral ar-
(1998) or Kramer and Eck (2000), and they both ticular contact at or near full extension of the joint,
differ from one another. So, although there have such as occurs in humans during the stereotypic
been main arguments made for a kinematically dis- loading patterns of normal gait. Apes have nearly
tinct gait, there is still no consensus on how their circular condylar profiles, with similar joint con-
gait differed, or what the costs in energy expendi- tours in all positions in the knee flexion-extension
ture or mobility would have been. cycle. This indicates that peak transarticular loads
A bent-knee posture is also inconsistent with the occurred at or near full knee extension in A. afaren-
distal femoral morphology of A. afarensis. The ex- sis, rather than in a bent-knee posture, during bipe-
panded calcaneal tuberosity of A. afarensis indicates dal progression, as in humans. Monkeys have an-
that initial contact during gait was a heel strike (see
teroposteriorly expanded knee joints, but this
also, Gebo, 1996), and that weight was borne on a
results from a deepening of the patellar surface and
single support limb (Latimer and Lovejoy, 1989).
minimal overlap between the patellar and tibial
Heel strike would have occurred with the knee at or
near full extension, as it in humans, and the knee joint surfaces (Fig. 4). The tibial surfaces are re-
would have been straightened further through mid- stricted to a posterior position, reflecting habitually
stance and late stance. The lateral lip of the patellar bent knees. Because A. afarensis individuals were
groove is higher than the medial one in both A. habitual bipeds, if the knee was adapted to being
afarensis specimens AL 129-1 and AL 288-1, and loaded in partial flexion at heel strike, we should see
differs markedly from the situation seen in apes, either no flattening, as muscular energy could be
despite the mediolaterally broad distal femur re- used to dissipate ground reaction forces, or else any
tained in A. afarensis (Fig. 5). AL 288-1 is slightly flattening should be oriented further posteriorly.
damaged along its superior patellar surface, which These data do not support the hypothesis that A.
often cannot be appreciated on casts. This elevated afarensis had a lower limb posture appreciably dif-
surface is consistent with the valgus angle, and with ferent from that of humans during bipedal gait.
significant quadriceps muscle contraction at or near Data suggesting different distributions of subchon-
full extension, as would occur from initial contact dral surface at the A. afarensis hip joint (MacLatchy,
through early preswing phases of bipedal gait. A. 1996) may reflect the different patterns of musculo-
afarensis also exhibits elliptical lateral femoral con- skeletal anatomy surrounding the hip joint rather
dyles with the flattest region on the distal surface, than different limb posture.
Another feature in which Australopithecus is pre- bilities, which are largely beyond the scope of this
sumed to have been more chimp-like than are hu- paper. Increasing body size may have played a part,
mans is in its talocrural joint. Based on the dimin- along with other selective pressures to modify pelvic
utive AL 288-1 talus and tibia, Latimer et al. (1987) form to accommodate childbirth for larger-brained
reported that the anteroposterior convexity of the infants (Tague and Lovejoy, 1986; Ruff, 1998). At
talar trochlea was more tightly curved than is that present, there is no clear refutation of the hypothe-
of humans or gorillas, matching only chimpanzees sis that the primitive traits in the A. afarensis skel-
among extant hominoids. Furthermore, when range eton compromised their bipedal ability.
of joint motion was estimated by articulating the
Continuing morphological refinement or stasis?
associated tibia, AL 288-1 had 2–3° greater range of
motion than seen in humans or gorillas (Stern and There is actually little fossil evidence to defini-
Susman, 1983), which they interpreted as advanta- tively answer this question. There is certainly not
geous for climbing in trees, suggesting arboreality in enough to accurately assess change in patterns of
A. afarensis. A new, larger talus from Hadar, AL variation over time. It appears, however, that the
147-30 (unpublished findings), has a flatter trochlea general pattern of postcranial morphology exhibited
than that of AL 288-1, with a subtended angle of within Australopithecus was essentially constant.
only 115°, considerably less than that of AL 288-1, There is little evidence so far to suggest that Aus-
which is 140° (Latimer et al., 1987). The new talus tralopithecus morphology continues to change over
falls within the human range (humans range from time and become more human-like, although it is
95–120°, and chimpanzees from 110 –145°. This does possible that there may have been minor modifica-
not necessarily indicate that large and small Hadar tions of the basic pattern in different species.
hominids differ in locomotor repertoire, because Broadly speaking, there is an Australopithecus pat-
these individuals do not exceed the range of varia- tern of morphology that changes appreciably only
tion within extant species. Thus this new fossil re- with the advent of Homo erectus/ergaster around 1.8
futes the hypothesis that the talocrural joint was mya.
distinct from that of extant humans, although the Within A. afarensis, the only taxon for which there
species range may have been lower. It is notable that is even a hope of assessing temporal change (as in
gorillas have a range of values from 90 –120°, like craniodental material; Lockwood et al., 2001), there
humans, suggesting an allometric effect (Latimer et is no apparent change over time postcranially. Com-
al., 1987). paring earlier and later Hadar specimens, there are
The relatively longer toes of A. afarensis (Stern no apparent differences in postcranial form (but see
and Susman, 1983; Susman et al, 1984; White and Senut, 1978, but see 1980; Tardieu, 1979, 1986a,b),
Suwa, 1987) have been suggested to imply a differ- and certainly none identified so far to be outside the
ent gait pattern. Whether or not the gait of A. afa- range of variation exhibited in a modern species. No
rensis would have looked unusual due to having other Australopithecus species has a sufficient num-
larger feet is uncertain. There are no associated ber of specimens or temporal resolution to observe
pedal and lower limb skeletons to assess relative potential change over time.
foot length empirically. Further, the variation Across australopithecine taxa, there are only
among extant humans with different relative foot weak hints of temporal trends to become less ape-
and toe lengths is considered normal intraspecific like and more human-like postcranially. The earliest
variation, and few researchers would argue that any Australopithecus species identified so far is A. ana-
humans are more or less effective bipeds as a con- mensis (Leakey et al., 1995, 1998; Ward et al.,
sequence. 1999a, 2001). Postcranially, A. anamensis is known
In summary, while several researchers have pos- from only the proximal and distal thirds of a tibia, a
ited a less efficient form of bipedality for A. afaren- distal humerus, a nearly complete radius, and a
sis, none has yet falsified the hypothesis that lower capitate and partial proximal manual phalanx. In
limb posture was not within the range of modern most ways, these bones closely resemble those of A.
humans. Furthermore, the various analyses fail to afarensis. From the tibia, we can infer that A. ana-
support a single mechanism by which they differ, mensis was a habitual biped: as in all other homi-
instead positing either different hip postures or nins, the A. anamensis tibia displays a diaphysis
movement during locomotion. Data are unclear that is oriented normal to the talocrural joint sur-
whether the ape-like aspects of the A. afarensis skel- face, rather than the varus angle found in apes (Fig.
eton diminished their efficiency as terrestrial bi- 6) (Latimer et al., 1987; Ward et al., 1999a). The
peds. While the detailed kinematic profile of A. afa- humerus, discovered long before it was attributed to
rensis individuals might differ in some ways from A. anamensis (Patterson and Howells, 1967), is in-
that of humans, there is no certainty that they distinguishable from that of A. afarensis (Feldes-
would have been less capable bipeds as a conse- man, 1982; Hill and Ward, 1988; Lague and
quence of their retained primitive traits. This then Jungers, 1996; Ward et al., 2001), despite sugges-
begs the question of why Homo altered the primitive tions that it is more like that of Homo (Senut and
hominin pattern, with its apparent mechanical im- Tardieu, 1985; Baker et al., 1998), as is the phalanx.
provements for bipedality. There are multiple possi- The radius is similar as well, and belonged to a
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
Fig. 6. Above, posterior views of distal tibias of Homo sapiens, that STW 573 had an abductable hallux. Observa-
Australopithecus anamensis (KNM-KP 29285), and Pan troglo-
dytes, oriented so that talocrural joint surfaces are horizontal. tion of the original specimen reveals that this spec-
Below, graph of angles of inclination relative to talar surface in imen does not differ from A. afarensis or from OH8
extant and fossil taxa (adapted from Latimer et al., 1987). All in joint morphology and orientation, however
hominins have vertically oriented tibial shafts relative to talar (Leakey 1960, 1961), which is attributed to Homo/
joint surface, whereas apes have sharply inclined tibial shafts,
placing knee well lateral to ankle in terrestrial plantigrade pos-
Australopithecus habilis (Leakey et al., 1964). A.
ture. africanus also has been suggested to have more ape-
like limb proportions than does A. afarensis
(McHenry and Berger, 1998), but Häusler (2001)
forearm that was longer than the longest one pre- noted that upper limb length to acetabulum size
served for A. afarensis (Heinrich et al., 1993). This does not differ between two partial skeletons of A.
suggests that the forearms of A. anamensis were at afarensis (Al 288-1) and A. africanus (STW 431).
least as long as those of A. afarensis, and almost Differences noted by McHenry and Berger (1998) in
assuredly longer for their body size than those of associated skeletons reflect the relatively large ra-
Homo. The capitate is poorly preserved, but sug- dial head of A. africanus (Häusler, 2001).
gests a more laterally facing second metacarpal In summary, A. africanus may have been slightly
facet than is seen in any other hominins, and in- more derived than was A. afarensis in most features
stead resembles the condition found in great apes. where the species differ. Because A. africanus is
The only place in which these taxa differ is the later in time (McKee, 1993; Walter, 1994; McKee et
capitate facet, reflecting rotational ability of the sec- al., 1995), this could indicate a directional trend. If
ond carpometacarpal joint (Leakey et al., 1998). Be- these taxa represent a single lineage, this might
cause it is likely that A. anamensis and A. afarensis signal disaptation in the traits that change and their
represent a single lineage, there is evidence of post- related soft tissues.
cranial change only in the hand, but that bipedality Australopithecus boisei is too poorly known post-
had been established by 4.2 million years ago. This cranially to compare. A. robustus, on the other hand,
suggests that the primitive traits seen in A. afaren- is known from a number of postcranial bones, al-
sis probably had been retained by bipedal hominins though many cannot be attributed to Australopithe-
for nearly a million years. cus with certainty, as Homo is also known from the
A. afarensis and A. africanus are similar postcra- same sites. The putative A. robustus hand bones are
nially in overall morphological pattern, although described as more human-like, with broader apical
there are some comparatively minor differences tufts on the terminal phalanges and flat first meta-
(Häusler, 2001 and references therein). When they carpal bases (Susman, 1988, 1989). Its ilium (SK
differ, A. africanus generally has slightly more hu- 3155) has been described as having a relatively
man-like morphology than does A. afarensis, but not wider and more cranially extensive iliac blade with a
larger auricular surface than those of A. africanus perhaps hint at the evolutionary significance of ar-
and A. afarensis (Brain et al., 1974; McHenry, 1975), boreality. Relatively few studies have investigated
but this variation may reflect body size and/or indi- this possibility. Data about actual behaviors will
vidual variation (McHenry, 1975). Other A. robustus come from traits that are phenotypically plastic, and
postcranial bones are not notably different from reflect an individual’s behavior pattern (Churchill,
those of A. afarensis or other Australopithecus spe- 1996; Lieberman, 1997). As noted above, one poten-
cies (Broom and Robinson, 1949; Napier, 1959, 1964; tial avenue of research is the investigation of diaph-
Robinson, 1970; Day and Scheuer, 1973; Brain et al., yseal structure in Australopithecus (Ruff, 1998; Ruff
1974; Susman, 1989; McHenry, 1994; Susman et al., et al., 1999), as it is developmentally sensitive.
2001). Suggested variation certainly does not ap- Because the derived signal for terrestrial bipedal-
proach the condition seen in Homo erectus/ergaster. ity is clear, we can hypothesize that not only had A.
No other Australopithecus species is known post- afarensis been selected to be bipeds, but that they
cranially. Postcrania from the Hata Member of the actually traveled bipedally. The pronounced femoral
Bouri Formation in Ethiopia cannot be definitively bicondylar angle indicates that A. afarensis actually
attributed to A. garhi, the only hominin identified at engaged in bipedal walking or running (Tardieu and
the site (Asfaw et al., 1999). However, these fossils Trinkaus, 1995; Duren, 1999). The flattened femoral
display a primitive, A. afarensis-like brachial index condyles may also reflect habitual loads in knee
but with a proportionately longer lower limb, sug- extension, as joints appear to be shaped during
gesting selection for increased lower limb length if grown by response to hydrostatic pressure in artic-
this hominin was a descendent of A. afarensis. ular cartilage (Frost, 1990a; Hamrick, 1999). Evi-
Thus, the basic pattern of postcranial anatomy dence for tree-climbing is less clear, but also not
exhibited by A. afarensis appears to persist for over thoroughly explored.
3 million years, suggesting that its locomotor adap- Coffing (1998) examined metacarpal diaphyseal
tation was stable, and not undergoing ongoing selec- robusticity in Australopithecus and extant homi-
tion for improved terrestrial competence. The slight noids. She argued that skeletal changes improving
differences between A. africanus and A. afarensis terrestrial competence in A. afarensis would have
might signal slight directional selection towards a decreased their arboreal capabilities. She predicted
Homo-like condition if they had an ancestor-descen-
that if A. afarensis still practiced arboreal behaviors,
dent relationship, which is far from certain. Simi-
they would have to have had even greater forelimb
larly, if the postcrania from the A. garhi site rep-
strength than extant apes. She did not explicitly
resent a descendent of A. afarensis, lower limb
discuss issues of genetic vs. epigenetic effects on
elongation may have occurred. These observations
diaphyseal form, but given assumptions about bone
are speculative, and meant only to point out possi-
bilities. If they were eventually supported by further modeling, it was implicit that individual behaviors
evidence, this might support a hypothesis of disap- were involved. Her analyses suggested that A. afa-
tation for some primitive traits of A. afarensis. rensis did indeed have stronger metacarpal diaphy-
The length of time over which the basic Australo- ses than would be expected for their body size and
pithecus pattern appears to have been retained bone lengths compared with those of modern hu-
seems to be the strongest evidence that primitive mans. Ruff (1998) reported that the femur was also
morphology retained an adaptive advantage for Aus- more robust than humans or apes, however, sug-
tralopithecus individuals, although it does not fal- gesting that their skeletons were more robust over-
sify the null hypothesis of nonaptation. If bipedality all than the modern taxa, rather than being tied to
began with late Miocene putative hominins like Sa- arboreality or bipedality. Still, this provides some
helanthropus and Orrorin, both about 6 million indirect support for Coffing (1998). Coffing (1998)
years old, it would have been around for 3 million implied that her hypothesis is mainly about upper
years before the appearance of A. afarensis. Even so, limb strength, but it could be interpreted to mean
it had been around for almost 1 million years since strength throughout the body.
A. anamensis. The general australopithecine body Indicators of muscle size and strength in A. afa-
plan remains for perhaps up to 1 million years ago, rensis tend to be large relative to modern humans,
until the disappearance of this species. If the prim- such as deltoid tuberosities (Aiello and Dean, 1990),
itive Australopithecus traits were disadvantageous, flexor muscle insertion sites manually and pedally
selection would have had ample time to eliminate or (Marzke, 1983; Stern and Susman, 1983; Susman et
alter them. If they were selectively neutral, we need al., 1984), and the peroneal groove on the fibula and
to explain why they never changed until the appear- peroneal trochlea on the calcaneus (Latimer and
ance of Homo. Lovejoy, 1989, 1990b). Indicators of relative muscu-
larity in all regions of the A. afarensis skeleton are
Did A. afarensis actually climb trees?
generally greater than in modern humans, as with
Another question to address would be whether or all premodern hominins (Ruff et al., 1993, 1999;
not we have enough evidence to assess whether A. Coffing, 1998). If overall muscularity was greater in
afarensis was actually climbing trees or not. This A. afarensis than in modern humans, it would not be
would be important to reconstruct behavior, and to possible to test whether this was to improve climb-
ing specifically, or for other reasons such as foraging Lovejoy, 1990b; Stern and Susman, 1983; White and
or defense. Suwa, 1987), and so the size of supports they could
Richmond (1998) and Paciulli (1995) conducted have grasped would be less. Even if their manual
cross-sectional growth studies of phalangeal curva- grasp was greater than that of humans, and their
ture in apes and humans. They both found that pedal grasp like that of the manual grasp of modern
curvature is greatest during the juvenile period, 2-year-old humans (Susman et al., 1984; Stern,
roughly at the time in which juveniles spend the 2000), we still cannot be sure that this was retained
greatest proportional amount of time engaging in for adaptively significant arboreal behaviors. They
arboreal behaviors. If their results are confirmed by would have been more competent in the trees than
other analyses, particularly longitudinal ones, this are typical humans, as they are much stronger and
would be a character indicating that at least juvenile had very slightly better mechanics with longer
A. afarensis spent time in the trees. Contrary to the arms, fingers, and toes. Any arboreal locomotion
results of phalangeal studies, Tardieu and Preuschoft would still necessarily have been fairly slow and
(1996) inferred that the morphology of developing deliberate, however, more for something like sleep-
epiphyseal plates was affected by behavior, and that ing in trees than for hunting or fleeing from preda-
the immature Hadar femora resemble those of hu- tors. Certainly females with infants would have had
mans, and not apes. This suggested to them that A. difficulty climbing trees, because without grasping
afarensis individuals were not climbing, as they halluces they would have had to hold onto their
lacked the apparent adaptations for stabilizing the infant with at least one arm. Still, sleeping in trees
epiphysis during arboreality. Duren (2001) also for safety is a potentially significant behavior that,
found significant links between epiphyseal orienta- at least in theory, could have selected for some rel-
tion and form and locomotion among catarrhines. atively weak climbing capabilities.
Another example of a trait that is clearly influ- In summary, studies of ontogenetically sensitive
enced by behavior to at least some degree is humeral morphology have shown that A. afarensis individu-
torsion (Martin and Saller, 1959; King et al., 1969; als walked bipedally, but do not lead to a consensus
Sarmiento, 1985; Pieper, 1998). As noted above, about A. afarensis locomotion. Relatively few studies
Australopithecus has less humeral torsion than do have been conducted so far, however. Research on
humans or extant great apes. This could be inter- the influences of individual activity patterns on the
preted as a series of evolutionary reversals or char- development of adult morphology is key to determin-
acter transformations from an ape-like ancestor to ing what behaviors A. afarensis individuals engaged
Australopithecus to human. However, this feature in over the course of their lifetime, and are well
may well be epigenetically influenced, as captive worth pursuing.
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; When using morphological features to make phy-
King et al., 1969; Sarmiento, 1985; Pieper, 1988). logenetic or behavioral inferences about fossil taxa,
Handball players (Pieper, 1988) and baseball pitch- we need to keep in mind the integrated nature of
ers (King et al., 1969) have higher levels of torsion anatomy (recent discussions in Witmer, 1995;
than other people. Because humeral torsion also is Churchill, 1996; Lieberman, 1997, 1999; Lovejoy et
influenced structurally by scapular position and el- al., 1999, 2000). Of course, though all we have are
bow joint orientation, via whatever mechanisms, the the bones of fossil animals, we need to bear in mind
fact that A. afarensis differs from humans and ex- that the growth and function of soft tissues can
tant apes in having less torsion could be related to influence skeletal form (Witmer, 1995, 1997). We
the inferred different shape of their thorax (Schmid, know that activity pattern can affect bone shape
1983; Jellema et al., 1993). Thus, lower humeral (e.g., Arkin and Katz, 1956; Carter and Wong, 1988;
torsion in A. afarensis could represent structural Ruff, 1992; Ruff et al., 1993, 1994; Trinkaus et al.,
differences resulting from selection for torso shape, 1991, 1994; Tardieu and Trinkaus, 1994; Churchill,
from different upper limb use, or both. These possi- 1996; Martin et al., 1998; Skerry, 2000), as can se-
bilities warrant further investigation. lection on soft tissues (e.g., Gibbs et al., 2002; Wit-
Finally, when assessing the likely behaviors of mer, 1995, 1997). We also know there may be genetic
Australopithecus, we can consider the capabilities and other developmental links among structures
evident in their morphology. Even if A. afarensis (e.g., Zelditch, 1987, 1988; Alberch, 1982; Cheverud,
spent time in the trees, without a grasping hallux 1984; Maynard Smith et al., 1985; Lieberman, 1997,
(White and Suwa, 1987; Latimer and Lovejoy, 1999; Hall, 1999; Tardieu, 1999), so that selection
1990b; but see Clarke and Tobias, 1995) they would for an aspect of one trait can directly impact the
have been significantly less agile than are apes and form of another. This is not to say, however, that
monkeys, especially in the case of females holding selection cannot independently modify structures,
infants. Despite the apparently slightly longer and only that it is possible that structures may experi-
more curved toes than are typical for modern hu- ence modifications concomitant with selection on a
mans, their toes were still shorter and straighter linked trait. The functional and evolutionary signif-
than those of apes (Bush et al., 1982; Latimer and icance of bone form can only be understood accu-
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
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 skeleton can result in changes elsewhere (Tague,
The existence of these effects and their potential 2002a). For example, a combination of Hoxa-11 and
consequences is not a new revelation, but has al- Hoxa-13 mutations can result in reduction of the
ways been verging on unobtainable information, and first ray and increased length of rays 2–5, mirroring
so by practical necessity is often ignored. changes thought to have occurred in apes. Hoxd-11
An example of integrated morphology is the shift can be responsible for a suite of alterations, includ-
in overall torso shape in apes and monkeys (Benton, ing reduced metacarpals 2–5, reduction of the ulnar
1965, 1976; Ward, 1991, 1993). Great apes have styloid process, and transformation of a sacral ver-
vertebral transverse processes that arise from the tebra into a lumbar one (Davis and Capecchi, 1994;
neural arch rather than the vertebral body, flaring Favier et al., 1995, 1996). A broadly similar suite of
iliac blades, and coronally oriented scapulae, along morphologies appears to differentiate hominins
with concomitant shifts in related muscular anat- from apes, suggesting the possibility of a single ge-
omy. Rather than positing that each of these fea- netic change resulting in multiple developmental
tures was under independent selective pressure, be- shifts. The extent to which a single gene is involved
cause they are spatially and structurally related remains to be determined, but pleiotropy is a tena-
with one another, and always correlated, they ap- ble hypothesis. As the details of these links and their
pear to represent related changes resulting from a effects on adult form continue to be worked out, it is
reorganization of the torso, in this case to enhance critical that we incorporate this type of information
the effectiveness of abduction-adduction movements into our morphological and phylogenetic interpreta-
of the arm for arm-hanging and forelimb-dominated tions.
arboreal activities. The most explicit attempt to assess and code the
Recent scientific progress is improving our ability types of interaction among tissues and structures
to incorporate pleiotropic and ontogenetic informa- via ontogeny and selection in determining form has
tion in paleontological interpretations. Discoveries been that of Lovejoy et al. (1999, 2000). They pro-
in the fields of genetics and developmental biology posed five trait types that differ in the degree to
have been rapidly increasing our knowledge about which they are acted upon directly or indirectly by
the control and ontogenetic mechanisms of structure selection, are influenced by selection on related
formation (e.g., Hinchcliffe, 1991; Wolpert, 1983; structures, or are epigenetically influenced by indi-
Hall, 1999; Cohn and Bright, 2000; Gilbert, 2000; vidual activity over a lifetime (Table 1). This classi-
Skerry, 2000; Hamrick, 2002; other articles in fication system represents a model to employ when
O’Higgens and Cohn, 2000). An interesting set of attempting to interpret evolutionary history or be-
examples of developmental genetic links among ap- havior in fossil taxa, and so should be useful for
pendicular and axial structures comes from studies assessing Australopithecus. By employing either
of Hox genes, as well as other gene systems such as this system, or at least the logic underlying it, we
Pax. Alterations in their expression appear to affect should be in a better position to more accurately
the condensation and proliferation of limb-bud mes- interpret early hominin morphology.
enchyme, and mutations in these genes generally The difficulty will often be in identifying the spe-
have multiple effects on the resulting skeleton cific influences on a trait, and classifying individual
(Davis and Capecchi, 1994; Favier et al., 1995, 1996; traits, as illustrated by some of the examples in
Fromental-Ramain et al., 1996). Such links can pro- Lovejoy et al. (1999, 2000). In addition, some char-
vide mechanisms whereby selection on one aspect of acters may fall into more than one type category,
having multiple influences, and so perhaps sending ior. They also suggest that different bones have dif-
us multiple signals. Still, using this general ap- ferent constraints on their form. Most recently, it
proach, we can construct testable hypotheses about was proposed that epiphyseal plate form is a greater
the functional and evolutionary relevance of charac- determinant of diaphyseal cross-sectional form than
ters, and test them using experimental approaches. is activity (Ohman and Lovejoy, 2001). Data sug-
Such tests might arise using locomotor studies, de- gest, however, that while within some taxa there
velopmental genetic and molecular biology, or the may be an effect of epiphyseal geometry on diaphy-
comparative method. The importance of this scheme seal midshaft shape, there is considerable variation
lies in its attempt to identify the influences on bone in this relationship, and it does not hold true within
form. or among taxa in metacarpals (Holden and Ward,
An excellent example of a trait whose influences unpublished data) or femur (Nalley and Ward, un-
currently are under intense scrutiny is long bone published data). It appears now that there may be
diaphyseal form. One bone mechanical theory states an inherent, genetically influenced initial shape de-
that certain levels of strain trigger bone-modeling termined in part by selection on joint form, which
responses, as bone models to maintain particular influences epiphyseal geometry. This geometry may
strain distributions necessary to perform necessary have a slight effect in diaphyseal cross-sectional
metabolic function while maintaining structural in- form. This initial form then may be modified by
tegrity (Martin et al., 1998 and references therein). activity pattern (Martin et al., 1998 and references
Using engineering beam theory, investigators have therein), especially early in life (Ruff et al., 1994).
inferred that because bones are subjected to bending Body proportions and muscle distributions about the
under normal physiological loading conditions, the bone affect patterns of bone strain, and ultimately
greatest tensile strain caused by bending should be diaphyseal form. It also appears that bone may not
located near midshaft. Tensile strain is thought to model to eliminate strain, but to enhance predict-
invoke the most significant modeling response in ability of strain, and even to maintain a certain level
bone. Operating on the assumption that bone mod- of strain with activity (Bertram and Biewener, 1983;
els to minimize tissue strain, researchers inferred Rubin, 1984). According to the scheme of Lovejoy et
that the plane in which maximum bending occurs al. (1999, 2000) (Table 1), long bone diaphyseal form
should have the greatest bending rigidity. Thus, the appears to be a mixture of trait types 1, 2, and 4.
amount of load to which a bone is subjected during The picture is complex, but this attention to the
growth should be reflected in its midshaft diaphy- determinants of diaphyseal form is exactly what is
seal cross-sectional geometry. This assumption was needed to determine the genetic and epigenetic in-
used to infer activity patterns in humans and other fluences on bony morphology, and any other ontoge-
primates (Ruff, 2000; Martin et al., 1998). netic or pleiotropic effects. Armed with such detailed
As this field of inquiry developed, it was gradually information, we will be better able to accurately
realized that other variables such as body shape are infer activity patterns from the skeleton. We will
influential in determining long bone form. It cer- also be in a better position to use morphological
tainly is becoming apparent that there is an age information to infer phylogeny and interpret pat-
effect on the responsiveness of bone to activity pat- terns of character transformation within a lineage.
tern, because mechanical sensitivity of the modeling Again, advances in our understanding of genetic
response appears to diminish as an individual ap- and other molecular influences on the development
proaches skeletal maturity (Frost, 1990a, b; Carter of adult form will help us develop and test more such
and Beaupré, 2001). Furthermore, some experimen- hypotheses, and improve the accuracy with which
tal strain gauge work suggests that contrary to the we interpret the fossil record.
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 If we want to understand how humans evolved,
loads incurred by walking or climbing (Demes et al., the operative question is finding out why our earli-
1998, 2001). It may be that patterns of muscle re- est relatives evolved as they did. All of our work to
cruitment, when counteracting ground reaction determine what A. afarensis individuals looked like
forces, may exert more relevant strain distributions and what they did, and how they evolved over time,
rather than simply the ground reaction vectors. provides the raw data with which to test hypotheses
However, the one animal that galloped in the study, about relationships between locomotion and other
incurring maximum strain values, did have peak aspects of a species’ biology, such as diet or social
strains that approached the orientation predicted by behavior.
bone sectional form (Demes et al., 2001). This may Since many hypotheses proposed to explain the
suggest that it is the peak strains only that stimu- evolution of bipedality revolve around diet and food
late diaphyseal modeling to improve bending rigid- acquisition (Du Brul, 1962; Hunt, 1994; Jolly, 1970;
ity near bone midshafts, altering their shapes. Prost, 1980; Wrangham, 1980; others summarized
These studies point to our need for caution when by Rose, 1991; Richmond et al., 2001), it is worth
using cross-sectional diaphyseal form to infer behav- considering links between the adoption of Australo-
pithecus bipedality and evidence of diet. A. anamen- tatively referred to robust Australopithecus: Omo
sis exhibits different dentognathic morphologies L40-19 (Howell and Wood, 1974; McHenry, 1976;
from those of earlier hominoids, and so appears to Day, 1978; Feldesman, 1979; McHenry and Te-
have had a different dietary specialization. A. ana- merin, 1979) and Olduvai OH 36 (Walker and
mensis shares thick enamel on its teeth with all Leakey, 1993; Aiello et al., 1999). They appear more
later hominins. It has a reduced anterior dentition. curved than do those of A. afarensis and A. africa-
Although not quite as much as seen in later homi- nus, or of those of Homo, and their proximal ends
nins, it is considerably more than in any earlier ape. also have some ape-like characteristics (Drapeau,
Its mandibular corpus was also not much stronger 2001). It is not yet clear, however, whether the hy-
than that of apes, and less robust that that of later pothesis can be falsified that the variation exhibited
hominins (Teaford and Ungar, 2000). Its jaw struc- by all Australopithecus ulnae exceeds that found in
ture was more ape-like than that of later hominins, any single extant species, much less genus.
however, with nearly parallel postcanine tooth rows, In summary, the heavy chewing adaptations seen
and a deep and receding mandibular symphysis, in A. garhi and other robust Australopithecus spec-
although the structure of the symphysis differs imens do not appear to be systematically linked with
slightly from that of apes. Thus there appear to be more human-like skeletons, although there may be a
changes in diet associated with Australopithecus, slight association. Admittedly, postcranial fossils
and thus far, with committed bipedality. Teaford are poorly known for most Australopithecus species.
and Ungar (2000) interpreted the A. anamensis mor- As more are discovered, this picture may change. At
phology as signaling a shift in emphasis from soft, present, however, while dietary adaptation may well
tough fruits to hard-object feeding. have accompanied the origin of Australopithecus,
If dietary and locomotor changes were necessarily from the limited data available, diet does not appear
dependent on one another in some fashion, we might to be an exclusive correlate of locomotor adaptation
expect to see them associated in some consistent among early hominins. Because of the poor fossil
pattern across bipedal hominins. While there appear record of postcranial anatomy of most Australopithe-
to be concomitant dietary and locomotor changes cus species, any such conclusions must remain ten-
associated with the origin of Australopithecus, there tative at present.
is no such evidence within the genus. The evidence Other hypotheses suggest that social behavior is
is extremely sparse from which to make such assess- linked with the acquisition of terrestrial bipedality
ments with any confidence so far. Still, from what (Lovejoy, 1981; Jablonski and Chaplin, 1993; others
little is preserved, evidence of dietary diversity summarized by Rose, 1991). One way in which social
among Australopithecus species does not, so far, ap- behavior can be reflected in the fossil record is in
pear to be associated with a consistent pattern of sexual dimorphism. While it is true that Australo-
locomotor specializations. A. africanus had slightly pithecus lost significant canine size dimorphism,
larger molars and reduced facial prognathism com- they retained a nearly 100% body size dimorphism.
pared with A. afarensis, suggesting continued spe- Males were almost double the size of females
cialization for hard object feeding (Teaford and Un- (McHenry, 1991, 1992, 1994), as evidenced by high
gar, 2000). A. africanus may have been even more levels of sizes represented in all species of Australo-
human-like than A. afarensis in some features, al- pithecus for which this is measurable (reviewed in
though there is little overall difference. Plavcan, 2000, 2001). No monogamous extant pri-
A. garhi had large molars like those of robust mate species has this much size dimorphism. All
australopithecines, a large sagittal keel, and other extant taxa with this much body size dimorphism
intense chewing adaptations (Asfaw et al., 1999). If are polygynous, either living in single- or multimale
the postcranial elements from the same site are groups, but with fairly intense levels of male-male
indeed those of A. garhi, it would appear to differ competition (Plavcan, 2000, 2001). Hence, while it is
from other Australopitheci postcranially as well, clear that relatively large canines had ceased to
with more human-like limb proportions than the confer reproductive advantage to male hominins,
other species for which this can be determined. The body size was apparently still valuable. Thus, the
only associated A. boisei postcranial fossil associated data do not support an association between monog-
with cranial remains is KNM-ER 1500. This fossil is amy and bipedality. The data do offer a link between
poorly preserved, but may have had more human- the cessation of canines as useful weapons in male-
like limb proportions than did A. afarensis (Leakey, male competition and the origins of committed bipe-
1973; Day et al., 1976; Leakey and Leakey, 1978; dality, however. Furthermore, this extreme body
Grausz et al., 1988). This appears similar to A. size dimorphism differs from the pattern seen in
garhi, and may suggest a link between hard-object humans and Pan, which all have much lower levels
feeding specialization and more human-like propor- of body mass dimorphism. Pan retains significant
tions. A. robustus, however, shows only slight evi- canine dimorphism, while humans do not. The data
dence for such an association. Since all postcrania suggest that Australopithecus social systems dif-
attributed to A. robustus are isolated, proportions fered from those seen in chimpanzes, bonobos, or
are difficult to assess. Two ulnae are unassociated humans. Similarities in social behavior shared be-
with any craniodental material, but have been ten- tween humans and chimpanzees on the one hand
(Wrangham, 1999), and humans and bonobos on the function. If this is not possible, we can try to use
other (Zihlman et al., 1978), appear to have evolved evidence of stasis or reconstructed behaviors to give
independently. us hints about the extent of stabilizing selection.
The nature of early hominin bipedality, and of Disaptation can be disproven by the continued
potential arboreal competence, bears on other be- maintenance or enhancement of a structure. To test
havioral reconstructions of early hominins. Chim- hypotheses about which behaviors A. afarensis indi-
panzee-like hunting would not be possible for Aus- viduals engaged in, we can consider the selective
tralopithecus, given their anatomical adaptations to regime suggested by their apomorphic morphology,
bipedality, even if they did use trees to some extent, but we also must attempt to identify traits that are
because it relies on a high level of arboreal compe- epigenetically sensitive to activity patterns.
tence. Thus, the importance of hunting for chimpan- Using this investigative framework, what we can
zees and humans (Stanford, 2001) appears to have infer about the selective regime acting on A. afaren-
been acquired independently. sis at this point is that the immediate ancestors of A.
Other hypotheses about early hominin behavior, afarensis, and probably A. anamensis and A. africa-
of which there are many, are not directly testable nus, had undergone intensive selective pressures to
using data from the early hominin record at present, be habitual terrestrial bipeds. This hypothesis is
but rely on other lines of evidence. Again, Ardipithe- supported by the numerous derived skeletal modifi-
cus, Orrorin, and Sahelanthropus will provide criti- cations from the likely ancestral condition. Mechan-
cal new information for testing hypotheses about the ical analyses suggest that these traits enhanced bi-
origins of bipedality by providing potentially new pedal locomotion, and that they are similar to
associations between locomotor, dietary, and social modern hominin bipeds. Furthermore, epigeneti-
behavioral adaptations in early hominins. They will cally sensitive traits, such as femoral bicondylar
also provide important information on the direction angles and epiphyseal contours, indicate that A. afa-
of morphological change in all regions of the skele- rensis actively engaged in bipedal locomotor behav-
ton, allowing us to assess the evolution and coevo- iors. Arboreal competence was reduced, indicating
lution of adaptive complexes in early hominins. that arboreality was of diminished importance for
individual survival and reproductive success. Most
SUMMARY AND CONCLUSIONS adaptations for arboreality likely present in the last
It is always the case that while fossils are the data common ancestor of apes and humans were altered
on hominin evolution, our theoretical approaches or lost. None was enhanced in response to changes
govern how we interpret them. The debate over lo- favoring bipedality, except perhaps for an increase
comotion in Australopithecus as it has been framed on overall strength (Coffing, 1998). Clearly, the re-
so far is becoming ineffective for helping us under- productive consequences of habitual bipedal travel
stand early hominin locomotor evolution. By identi- were considerable.
fying the causes of this debate and reframing the Moreover, the massive rearrangement of bone and
questions we ask of the fossils, we are in a better joint morphology and orientation implies that sub-
position to make progress. Some researchers have stantial loads were incurred while traveling bipe-
been concerned with attempting to reconstruct the dally. Extant apes are capable facultative bipeds,
selective regime that shaped A. afarensis, or why it being able to travel short distances during food-
evolved as it did. Others have been more concerned gathering episodes on two feet (Hunt, 1994). Their
with reconstructing individual activity patterns, or ability to climb trees is more important to them in
what they were like. Both approaches have value for terms of reproductive success, however, so apes have
developing a more complete understanding of the not been selected to modify their skeletons to be-
early radiations of hominins. We also need to remain come better bipeds. The selective consequences of
aware that some details about both research ques- problems that might stem from a musculoskeletal
tions will be beyond the limit of resolution allowed system poorly designed for bipedality, such as back
by the fossil record. problems or joint pain, are minimal in very short-
By clearly acknowledging the questions we are distance locomotor bouts. On the other hand, the
asking about the fossils, we can then use the data fitness of an animal traveling longer distances more
available to develop tests of hypotheses about adap- regularly, at high speed, or for particularly repro-
tation and/or behavior. Studies of adaptation must ductively valuable reasons (e.g., inter- or intraspe-
start with a reliable phylogeny incorporating living cific competition, or carrying), would be in jeopardy
and fossil hominoids. From this, vectors of morpho- with any such maladies. For this reason, the only
logical change can be identified, and with accompa- scenario that would select for the major alterations
nying biomechanical and comparative analyses, se- hominins underwent is if bipedality was employed
lective regimes can be interpreted. To test whether for more than simply standing and feeding, or walk-
primitive retentions were retained by stabilizing se- ing very short distances. The adaptive importance of
lection for maintenance of an ancestral behavior, bipedal travel is highlighted by the loss of the many
like climbing trees, we must determine whether the advantages of arboreal traits, in particular a grasp-
primitive morphology compromised the derived ing hallux, for use in climbing trees with speed and
agility for feeding, hunting, or predator escape, or rate phylogenetic reconstructions by allowing us to
for infants being able to cling to their mothers’ fur. make more appropriate character choices for our
This is not to say that using trees to some extent analyses.
was not necessarily selectively valuable for A. afa- The extent to which A. afarensis was arboreal has
rensis, but this assumption is difficult to test. It is implications for interpreting the pattern of natural
almost certain that A. afarensis individuals would selection that shaped the early part of our lineage.
have been more capable climbers than are most Recent claims for locomotor diversity among early
modern humans. They were smaller and relatively hominin species (Berger and Tobias, 1996; Clarke
stronger. They retained primitive features, such as and Tobias, 1995; McHenry and Berger, 1998) and
slightly longer arms, hands, and feet, that would the recovery of new, earlier fossils (White et al.,
have made them slightly more competent in the 1994; Haile-Selassie, 2001; Senut et al., 2001; Bru-
trees than are modern humans, but still consider- net et al., 2002) underscore the importance of find-
ably less so than any ape. The issue is whether or ing ways to more precisely interpret early hominin
not these features were actively maintained for positional behaviors. In addition, our understanding
climbing by causing individuals who lacked them, or of Australopithecus locomotor behavior is important
in whom they were more poorly developed, to leave for understanding the transition to Homo. If austra-
fewer descendents than those who did. Particularly
lopithecines and other early hominins were partly
in light of the strong directional signal away from
arboreal, postcranial changes seen in Homo erectus/
arboreality towards bipedality, it is difficult to dis-
ergaster might be due to a shift towards full bipedal-
prove the null hypothesis that these traits remained
as secondary nonaptations. There is no conclusive ity. On the other hand, if the ancestors of Homo were
evidence yet that the retained features of Australo- already fully bipedal, the changes in the Homo skel-
pithecus compromised its effectiveness as a biped, eton must have been due to other factors, such as an
but many researchers support this idea. The shape increase in efficiency due to walking longer dis-
of the femoral condyles and the bicondylar angle do tances or running, and/or selection for body size,
not support the hypothesis that Australopithecus throwing, tool use, and transport, or any number of
walked with a bent knee and hip, a position further other possibilities. Until we find a way to resolve
supported by modeling. this ongoing debate over the importance of arbore-
The strongest support for a hypothesis of stabiliz- ality in A. afarensis and other early hominins, we
ing selection at the moment is the apparently long will have a difficult time characterizing the impor-
period over which the Australopithecus suite of fea- tant transition (or transitions) involving postcranial
tures remained with little apparent modification. anatomy that shaped our lineage.
Certainly with the appearance of Homo erectus/er-
gaster, the hominin postcranial skeleton and proba- ACKNOWLEDGMENTS
bly muscular system underwent significant changes.
I thank Dave Begun, Mark Collard, Deborah Cun-
Before this time, however, despite an increasing dis-
ningham, Michelle Drapeau, Mark Flinn, Anne
cussion of postcranial variation among Australo-
pithecus species, there seems to be only a hint of a Holden, Amy Judd, Bill Kimbel, Bruce Latimer, Thi-
slight trend toward more “human-like” anatomy erra Nalley, Jason Organ, Brian Richmond, and
over time prior to 1.8 million years ago, and even Alan Walker for helpful discussions about the con-
this is a very tentative observation. cepts in this paper and sharing information. I thank
What we can say about the behavior of A. afaren- Lee Berger, Ron Clarke, Don Johanson, Bill Kimbel,
sis is that they were habitual bipeds, based on trait Bruce Latimer, Meave Leakey, Steve Leigh, Brian
polarities and epigenetically sensitive traits influ- Richmond, Philip Tobias, and the staffs of the Cleve-
enced by behavior, such as femoral bicondylar angle. land Museum of Natural History, National Muse-
Behavioral indicators of arboreality are unclear. ums of Kenya, the Transvaal Museum, National
Studies of phalangeal curvature may hint at tree- Museums of Ethiopia, the University of the Witswa-
climbing behavior, but more research is needed to tersrand, and the Institute of Human Origins for
support or refute this hypothesis. The robusticity of access to fossil, comparative skeletal, and cadaver
their skeletons may also prove to be related to arbo- specimens. I also thank Chris Ruff for inviting me to
real behaviors, but this has not been clearly demon- contribute this manuscript, and Martin Häusler,
strated yet. Studies of kinematic characteristics of Dan Lieberman, Henry McHenry, Chris Ruff, and
A. afarensis gait patterns have produced conflicting an anonymous reviewer for helpful comments and
results. Continued elucidation of the genetic, devel- suggestions.
opmental, and epigenetic bases for morphological
features and character complexes will be of critical LITERATURE CITED
importance in testing hypotheses about the actual
Abitbol MM. 1995. Lateral view of Australopithecus afarensis:
day-to-day behaviors of Australopithecus individu-
primitive aspects of bipedal positional behavior in the earliest
als. This will also help us explore the current uses to hominids. J Hum Evol 28:211–229.
which primitive traits of A. afarensis were put. In Aiello LC, Dean C. 1990. An introduction to human evolutionary
addition, these data will help us make more accu- anatomy. London: Academic Press.
Aiello LC, Wood B, Key C, Lewis M. 1999. Morphological and Berger LR, Tobias PV. 1996. A chimpanzee-like tibia from Sterk-
taxonomic affinities of the Olduvai ulna (OH 36). Am J Phys fontein, South Africa and its implications for interpretations of
Anthropol 109:89 –110. bipedalism in Australopithecus africanus. J Hum Evol 30:343–
Alberch P. 1982. Developmental constraints in evolutionary pro- 348.
cesses. In: Bonner JT, editor. Evolution and development. Ber- Bertram JEA, Biewener A. 1988. Bone curvature: sacrificing
lin: Springer-Verlag. p 313–332. strength for load predictability? J Theor Biol 131:75–92.
Arkin AM, Katz JF. 1956. The effects of pressure on epiphyseal Bock WJ. 1980. The definition and recognition of biological adap-
growth: the mechanism of plasticity of growing bone. J Bone tation. Am Zool 20:217–227.
Joint Surg [Am] 38:1056 –1076. Brain CK, Vrba ES, Robinson JT. 1974. A new hominid innomi-
Arnold SJ. 1983. Morphology, performance and fitness. Am Zool nate bone from Swartkrans. Ann Transvaal Mus 29:55– 66.
23:347–361. Brooks DR, MacLennan DA. 1991. Phylogeny, ecology and behav-
Asfaw B, White TD, Lovejoy CO, Latimer B, Simpson S, Suwa G. ior: a research program in comparative biology. Chicago: Uni-
1999. Australopithecus garhi: a new species of early hominid versity of Chicago Press.
from Ethiopia. Science 284:629 – 635. Broom R. 1943. An ankle-bone of the ape-man Paranthropus
Baker EW, Malyango AA, Harrison T. 1998. Phylogenetic rela- robustus. Nature 152:689 – 690.
tionships and functional morphology of the distal humerus Broom R, Robinson JT. 1949. A new type of fossil man. Nature
from Kanapoi, Kenya. Am J Phys Anthropol [Suppl] 26:66. 164:322–323.
Baum DA, Larson A. 1991. Adaptation reviewed: a phylogenetic Broom R, Robinson JT. 1950. Man contemporaneous with the
methodology for studying character macroevolution. Sys Zool Swartkrans ape-man. Am J Phys Anthropol 8:151–156.
40:1–18. Broom R, Schepers GWH. 1946. The South African ape-men: the
Beard KC, Teaford MF, Walker A. 1986. New wrist bones of Australopithecinae. Trans Mus Mem 2:1–272.
Proconsul africanus and P. hyanzoc from Rusinga Island, Ke- Broom R, Robinson JT, Schepers GW. 1950. Sterkfontein ape-
nya. Folia Primatol 47:97–118. man, Plesianthropus. Pretoria: South Africa.
Begun DR. 1992. Miocene fossil hominids and the chimp-human Bush ME, Lovejoy CO, Johanson DC, Coppens Y. 1982. Hominid
clade. Science 247:1929 –1933. carpal, metacarpal and phalangeal bones recovered from the
Begun DR. 1993. New catarrhine phalanges from Rudabanya Hadar formation: 1974 –1977 collections. Am J Phys Anthropol
(northeastern Hungary) and the problem of parallelism and 57:651– 678.
convergence in hominoid postcranial morphology. J Hum Evol Carpenter K, Smith MM. 2001. Forelimb osteology and biome-
24:373– 402. chanics of Tyrannosaurus rex. In: Tanke DH, Carpenter K,
Begun DR. 1994. Relations among the great apes and humans: editors. Mesozoic vertebrate life. Bloomington: Indiana Univer-
new interpretations based on the fossil great ape Dryopithecus. sity Press. p 90 –116.
Yrbk Phys Anthropol 37:11– 63. Carter DR, Beaupré GS. 2001. Skeletal function and form: mech-
Begun DR. 1999. Hominid family values: morphological and mo- anobiology of skeletal development, aging and regeneration.
lecular data on relations among the great apes and humans. In: Cambridge: Cambridge University Press.
Parker ST, Mitchell RW, Miles HL, editors. The mentalities of Carter DR, Wong M. 1988. The role of mechanical loading histo-
gorillas and orangutans. Cambridge: Cambridge University ries in the development of diarthrodial joints. J Orthop Res
Press. p 3– 42. 6:804 – 816.
Begun DR, Kordos L. 1997. Phyletic affinities and functional Cartmill M. 1994. A critique of homology as a morphological
convergence in Dryopithecus and other Miocene and living concept. Am J Phys Anthropol 94:111–123.
hominids. In: Begun DR, Ward CV, Rose MD, editors. Function, Cartmill M, Schmitt D. 1996. Pelvic rotation in human walking
phylogeny, and fossils: Miocene Hominoid evolution and adap- and running: implications for early hominid bipedalism. Am J
tations. New York: Plenum Press. p 291–316. Phys Anthropol [Suppl] 22:81.
Begun DR, Ward CV, Rose MD. 1997a. Events in hominoid evo- Chagnon NA. 1997. Yanomamo. Fort Worth: Harcourt Brace.
lution. In: Begun DR, Ward CV, Rose MD, editors. Function, Chan L-K. 1997. Thoracic shape and shoulder biomechanics in
phylogeny, and fossils: Miocene Hominoid evolution and adap- primates. Ph.D. dissertation, Duke University, Durham, NC.
tations. New York: Plenum Press. p 389 – 415. Cheverud JM. 1984. Quantitative genetics and developmental
Begun DR, Ward CV, Rose MD, editors. 1997b. Function, phylog- constraints on evolution by selection. J Theor Biol 110:155–171.
eny and fossils: Miocene Hominoid evolution and adaptations. Chopra SRK. 1962. The innominate bone of the Australopitheci-
New York: Plenum Press. nae and the problem of erect posture. Bibl Primatol 1:93.
Benton R. 1965. Morphological evidence for adaptations within Churchill SE. 1996. Particulate versus integrated evolution of the
the epaxial region of the primates. In: Vagtborg H, editor. The upper body in Late Pleistocene humans: a test of two models.
baboon in medical research. Houston: University of Texas Am J Phys Anthropol 100:559 –583.
Press. p 10 –20. Clarke RJ, Tobias PV. 1995. Sterkfontein Member 2 foot bones of
Benton RS. 1976. Structural patterns in the Pongidae and Cer- the oldest South African hominid. Science 269:521–524.
copithecidae. Yrbk Phys Anthropol 18:65– 88. Coffing KE. 1998. The metacarpals of Australopithecus afarensis:
Berge C. 1984. Multivariate analysis of the pelvis of hominids and locomotor and behavioral implications of cross-sectional geom-
other extant primates: implications for the locomotion and sys- etry. Ph.D. Dissertation, Johns Hopkins University, Baltimore,
tematics of the different species of australopithecines. J Hum MD.
Evol 13:555–562. Coffing KE. 1999. Paradigms and definitions in early hominid
Berge C. 1991. Quelle est la signification fonctionnelle du pelvis locomotion research. Am J Phys Anthropol [Suppl] 28:109 –110.
très large d’Australopithecus afarensis (AL 288-1)? In: Senut B, Coffing KE, HM McHenry. 2000. Clades and hominid postcranial
Coppens Y, editors. Origine(s) de la bipédie chez les Hominidés. fossils. Am J Phys Anthropol 30:127.
Paris: CNRS. p 113–120. Cohn MJ, Bright PE. 2000. Development of vertebrate limbs:
Berge C. 1994. How did the australopithecines walk? A biome- insights into pattern, evolution and dysmorphogenesis. In:
chanical study of the hip and thigh of Australopithecus afaren- O’Higgens P, Cohn MJ, editors. Development, growth and evo-
sis. J Hum Evol 26:259 –273. lution: implications for the study of the hominid skeleton. San
Berge C, Kazmierczak JB. 1986. Effects of size and locomotor Diego: Academic Press. p 1–28.
adaptations on the hominid pelvis: evaluation of australo- Collard M, Wood B. 2000. How reliable are human phylogenetic
pithecine bipedality with a new multivariate method. Folia hypotheses? Proc Natl Acad Sci USA 97:5003–5006.
Primatol (Basel) 46:185–204. Crompton RH, Li Y, Wang W, Günther M, Savage R. 1998. The
Berge C, Ponge J-F. 1983. Les caractéristiques du bassin des mechanical effectiveness of erect and “bent-hip, bent-knee” bi-
australopithèques: sont-elles dues à une bipédie de type hu- pedal walking in Australopithecus afarensis. J Hum Evol 35:
main? Bull Mem Soc Anthropol Paris 10:335–354. 55–74.
Dainton M, Macho GA. 1999. Did knuckle-walking evolve twice? Feldesman MR. 1979. Further morphometric studies of the ulna
J Hum Evol 36:171–194. from the Omo Basin, Ethiopia. Am J Phys Anthropol 51:409 –
Dart RA. 1925. Australopithecus africanus: the man-ape of South 416.
Africa. Nature 115:195. Feldesman MR. 1982. Morphometric analysis of the distal hu-
Dart RA. 1949a. The first pelvic bones of Australopithecus merus of some Cenozoic catarrhines: the Late Divergence hy-
prometheus: preliminary note. Am J Phys Anthropol 7:255– pothesis revisited. Am J Phys Anthropol 59:73–95.
257. Felsenstein J. 1985. Phylogenies and the comparative method.
Dart RA. 1949b. Innominate fragments of Australopithecus Amer Nat 125:1–15.
prometheus. Am J Phys Anthropol 7:301–334. Fromental-Ramain C, Warot X, Messadecq N, Le Meur M, Dollé
Dart RA. 1958. A further adolescent australopithecine ilium from P, Chambon P. 1996. Hoxa-13 and Hoxd-13 play a crucial role
Makapansgat. Am J Phys Anthropol 16:437– 479. in the patterning of the limb autopod. Development 122:2997–
Davis AP, Capecchi MR. 1994. Axial homeosis and appendicular 3011.
skeleton defects in mice with targeted disruption of Hoxd-11. Frost HM. 1979. A chondral modeling theory. Calcif Tissue Int
Development 120:2187–2198. 28:181–200.
Day MH. 1978. Functional interpretations of the morphology of Frost HM. 1990a. Skeletal structural adaptations to mechanical
postcranial remains of early African hominids. In: Jolly C, usage (SATMU): 1. Redefining Wolff’s law: the bone remodeling
editor. Early hominids of Africa. New York: St. Martin’s Press. problem. Anat Rec 226:403– 413.
p 311–345. Frost HM. 1990b. Skeletal structural adaptations to mechanical
Day MH, Scheuer JL. 1973. SKW 14147: a new hominid meta- usage (SATMU): 2. Redefining Wolff’s law: the remodeling
carpal from Swartkrans. J Hum Evol 2:429 – 438. problem. Anat Rec 226:414 – 422.
Day MH, Wickens EH. 1980. Laetoli Pliocene hominid footprints Frost HM. 1994. Perspectives: a vital biomechanical model of
and bipedalism. Nature 286:385–387. synovial joint design. Anat Rec 240:1–18.
Day MH, Wood BA. 1969. Hominoid tali from East Africa. Nature Frumhoff PC, HK Reeve. 1994. Using phylogenies to test hypoth-
222:591–592. eses of adaptation: a critique of some current proposals. Evo-
Day MH, Leakey REF, Walker AC, Wood BA. 1976. New homin- lution 48:172–180.
ids from East Turkana, Kenya. Am J Phys Anthropol 45:369 – Gans C. 1966. Some limitations and approaches to problems in
436. functional anatomy. Folia Biotheor 6:41–50.
Deloison Y. 1985. Comparative study of calcanei of primates and Gebo D. 1996. Climbing, brachiation, and terrestrial quadrupe-
Pan-Australopithecus-Homo relationships. In: Tobias PV, edi- dalism: historical precursors of hominid bipedalism. Am J Phys
tor. Hominid evolution: past, present and future. New York: Anthropol 101:55–92.
Alan R. Liss. p 143–147. Gebo D, MacLatchy L, Kityo R, Deino A, Kingston J, Pilbeam D.
Deloison Y. 1991. Les australopithèques marchaient-ils comme 1997. A hominoid genus from the Early Miocene of Uganda.
nous? In: Senut B, Coppens Y, editors. Origine(s) de la bipédie
Science 276:401– 404.
chez les Hominidés. Paris: CNRS. p 177–186.
Gibbs S, Collard M, Wood B. 2002. Soft tissue anatomy of the
Deloison Y. 1992. Articulation cunéométatarsienne de l’hallux
extant hominoids: a review and phylogenetic analysis. J Anat
considérée comme un des éléments déterminants de la forme de
200:3– 49.
locomotion à partir de son anatomie osseuse. Comparison entre
Gilbert SF. 2000. Developmental biology, 6th ed. Sunderland,
l’australopithéque, l’homme et le chimpanzÉ. C R Acad Sci
MA: Sinauer Associates.
Paris II 314:1379 –1385.
Gould SJ, Lewontin RC. 1979. The spandrels of San Marco and
Demes AB, Stern JT, Hausman JR, Larson SG, McLeod KJ,
the Panglossian paradigm: a critique of the adaptationist pro-
Rubin CT. 1998. Patterns of strain in the macaque ulna during
gramme. Proc R Soc Lond [Biol] 205:581–598.
functional activity. Am J Phys Anthropol 106:87–100.
Demes AB, Qin Y-X, Stern JT, Larson SG, Rubin CT. 2001. Gould SJ, Vrba ES. 1982. Exaptation—a missing term in the
Patterns of strain in the macaque tibia during functional ac- science of form. Paleobiology 8:4 –15.
tivity. Am J Phys Anthropol 116:257–265. Grausz HM, Leakey RE, Walker A, Ward CV. 1988. Associated
Descola P. 1986a. In the society of nature: a native ecology in cranial and postcranial bones of Australopithecus boisei. In:
Amazonia. Cambridge: Cambridge University Press. Grine FE, editor. Evolutionary history of the “robust” austra-
Descola P. 1986b. The spears of twilight: life and death in the lopithecines. New York: Aldine de Gruyter. p 127–132.
Amazon jungle. New York: New Press. Haile-Selassie Y. 2001. Late Miocene hominids from the Middle
Drapeau MS. 2001. Functional analysis of the associated partial Awash, Ethiopia. Nature 412:178 –181.
forelimb skeleton from Hadar, Ethiopia (AL 438-1). Ph.D. dis- Hall BK. 1999. Evolutionary developmental biology, 2nd ed. Bos-
sertation, University of Missouri-Columbia. ton: Kluwer.
Du Brul EL. 1962. The general phenomenon of bipedalism. Am Hamrick MW. 1999. A chondral modeling theory revisited. J
Zool 2:205–208. Theor Biol 201:201–208.
Duncan AS, Kappelman J, Shapiro LJ. 1994. Metatarsophalan- Hamrick MW. 2002. Evolution and development of the primate
geal joint function and positional behavior in Australopithecus limb skeleton. Evol Anthropol 11:94 –107.
afarensis. Am J Phys Anthropol 93:67– 82. Harrison T. 1986. A reassessment of the phylogenetic position of
Duren DL. 1999. Developmental determinants of femoral mor- Oreopithecus Gervais. J Hum Evol 15:541–583.
phology. M.A. thesis, Kent State University, Kent, OH. Harvey PH, Pagel MD. 1991. The comparative method in evolu-
Duren DL. 2001. Physeal orientation, form and function: relation- tionary biology. Oxford: Oxford University Press.
ships with primate locomotor Behavior. Ph.D. dissertation, Häusler MF. 2001. New insights into the locomotion of Australo-
Kent State University, Kent, OH. pithecus africanus: implications of the partial skeleton STW
Duren DL, Ward CV. 1995. Femoral physeal plate angles and 431 (Sterkfontein, South Africa). Ph.D. dissertation, Univer-
their relationship to bipedality. Am J Phys Anthropol [Suppl] sität Zürich.
20:86. Heinrich RE, Rose MD, Leakey RE, Walker A. 1993. Hominid
Evans FG, Krahl VE. 1945. The torsion of the humerus: a phylo- radius from the middle Pliocene of Lake Turkana, Kenya. Am J
genetic survey from fish to man. Am J Anat 76:303–337. Phys Anthropol 92:139 –148.
Favier B, Le Meur M, Chambon P, Dollé P. 1995. Axial skeleton Hill A, Ward S. 1988. Origin of the Hominidae: the record of
homeosis and forelimb malformations in Hoxd-11 mutant mice. African large hominoid evolution between 14 My and 4 My. J
Proc Natl Acad Sci USA 92:310 –314. Hum Evol 31:49 – 83.
Favier B, Rijli FM, Fromental-Ramain C, Fraulob V, Chambon P, Hinchcliffe JR. 1991. Developmental approaches to the problem
Dollé P. 1996. Functional cooperation between the non-paralo- of transformation of limb structure in evolution. In: Hinchcliffe
gous genes Hoxa-10 and Hoxd-11 in the developing forelimb JR, editor. Developmental patterning of the vertebrate limb.
and axial skeleton. Development 122:449 – 460. New York: Plenum. p 313–323.
Howell FC, Wood BA. 1974. Early hominid ulna from the Omo Larson SG. 1996. Estimating humeral torsion on incomplete fos-
Basin, Ethiopia. Nature 249:174 –176. sil anthropoid humeri. J Hum Evol 31:239 –257.
Hunt KD. 1994. The evolution of hominid bipedality: ecology and Larson SG. 1998. Parallel evolution in the hominoid trunk and
functional morphology. J Hum Evol 26:183–202. forelimb. Evol Anthropol 6:87–99.
Hürzeler J. 1960. The significance of Oreopithecus in the geneal- Latimer B. 1983. The anterior foot skeleton of Australopithecus
ogy of man. Triangle 4:164 –174. afarensis. Am J Phys Anthropol 60:217.
Inouye SE. 1994. Ontogeny of knuckle-walking hand postures in Latimer B. 1991. Locomotor adaptations in Australopithecus afa-
African apes. J Hum Evol 26:459 – 485. rensis: the issue of arboreality. In: Senut B, Coppens Y, editors.
Jablonski NG, Chaplin G. 1993. Origin of habitual terrestrial Origine(s) de la bipédie chez les Hominidés. Paris: CNRS.
bipedalism in the ancestor of the Hominidae. J Hum Evol p 169 –176.
24:259 –280. Latimer B, Lovejoy CO. 1989. The calcaneus of Australopithecus
Jellema L, Latimer B, Walker A. 1993. The rib cage. In: Walker A, afarensis and its implications for the evolution of bipedality.
editor. The Nariokotome Homo erectus skeleton. Cambridge, Am J Phys Anthropol 78:369 –386.
MA: Harvard University Press. p 294 –325. Latimer B, Lovejoy CO. 1990a. Metatarsophalangeal joints of
Johanson DC, Lovejoy CO, Kimbel WH, White TD, Ward SC, Australopithecus afarensis. Am J Phys Anthropol 83:13–24.
Bush ME, Latimer BM, Coppens Y. 1982a. Morphology of the Latimer B, Lovejoy CO. 1990b. Hallucal tarsometatarsal joint in
Pliocene partial hominid skeleton (A. L. 288-1) from the Hadar Australopithecus afarensis. Am J Phys Anthropol 82:125–133.
formation, Ethiopia. Am J Phys Anthropol 57:403– 452. Latimer B, Ward CV. 1993. The thoracic and lumbar vertebrae.
Johanson DC, Taieb M, Coppens C. 1982b. Pliocene hominids In: Walker A, Leakey RE, editors. The Nariokotome Homo
from the Hadar formation, Ethiopia (1973–1977): stratigraphic, erectus skeleton. Cambridge, MA: Harvard University Press.
chronologic, and paleoenvironmental contexts, with notes on p 266 –293.
hominid morphology and systematics. Am J Phys Anthropol Latimer B, Ohman JC, Lovejoy CO. 1987. Talocrural joint in
57:373– 402. African hominoids: implications for Australopithecus afarensis.
Jolly CJ. 1970. The seed-eaters: a new model of hominid differ- Am J Phys Anthropol 74:155–175.
entiation based on a baboon analogy. Man 5:1–22. Lauder GV. 1995. On the inference of function from structure. In:
Jolly CJ. 2001. A proper study for mankind: analogies from the Thomason JJ, editor. Functional morphology in vertebrate pa-
papionin monkeys and their implications for human evolution. leontology. Cambridge: Cambridge University Press. p 1–18.
Yrbk Phys Anthropol 44:177–204. Lauder GV. 1996. The argument from design. In: Rose MR,
Jungers WL. 1982. Lucy’s limbs: skeletal allometry and locomo- Lauder GV, editors. Adaptation. San Diego: Academic Press.
tion in Australopithecus afarensis. Nature 297:676 – 678. p 55–92.
Jungers W. 1984. Aspects of size and scaling in primate biology Leakey LSB. 1960. Recent discoveries at Olduvai Gorge. Nature
with special reference to the locomotor skeleton. Yrbk Phys 188:1050 –1052.
Anthropol 27:73–94.
Leakey LSB. 1961. New finds at Olduvai Gorge. Nature 189:649 –
Jungers WL. 1991. A pygmy perspective on body size and shape in
Australopithecus afarensis (A.L. 288-1, “Lucy”). In: Senut B,
Leakey LSB, Tobias PV, Napier JR. 1964. A new species of the
Coppens Y, editors. Origine(s) de la bipédie chez les Hominidés.
genus Homo from Olduvai Gorge. Nature 202:7–9.
Paris: CNRS. p 215–224.
Leakey MD, Hay RL. 1979. Pliocene footprints in the Laetolil
Jungers WL, Stern JT. 1983. Body proportions, skeletal allometry
Beds at Laetoli, Northern Tanzania. Nature 278:317–323.
and locomotion in the Hadar hominids: a reply to Wolpoff. J
Leakey MG, Leakey RE. 1978. Koobi Fora research project, vol-
Hum Evol 12:673– 684.
ume 1. Oxford: Clarendon Press.
Kay RF. 1975. The functional adaptations of primate molar teeth.
Leakey MG, Feibel CS, MacDougall I, Walker A. 1995. New
Am J Phys Anthropol 43:195–215.
Kay RF, Covert HH. 1984. Anatomy and behaviour of extinct four-million-year-old hominid species from Kanapoi and Allia
primates. In: Chivers DJ, Wood, A Bilsborough BA, editors. Bay, Kenya. Nature 376:565–571.
Food acquisition and processing in primates. New York: Ple- Leakey MG, Feibel CS, MacDougall I, Ward CV, Walker A. 1998.
num Press. p 467–508. New specimens and confirmation of an early age for Australo-
Kay RF, Hiiemae KM. 1974. Jaw movement and tooth use in pithecus anamensis. Nature 363:62– 66.
recent and fossil primates. Am J Phys Anthropol 40:227–256. Leakey RE. 1973. Further evidence of Lower Pleistocene homin-
Kay RF, Ungar PS. 1997. Dental evidence for diet in some Mio- ids from East Rudolf, North Kenya, 1972. Nature 237:170 –173.
cene catarrhines with comments on the effects of phylogeny on Leakey RE, Leakey MG, Walker AC. 1988. Morphology of Afro-
the interpretation of adaptation. In: Begun DR, Ward CV, Rose pithecus turkanensis from Kenya. Am J Phys Anthropol 76:
MD, editors. Function, phylogeny, and fossils: Miocene Homi- 289 –307.
noid evolution and adaptations. New York: Plenum Press. Le Gros Clark WE. 1947. Observations on the anatomy of the
p 131–151. fossil Australopithecinae. J Anat 81:300 –333.
Kern HH, Straus WL. 1949. The femur of Plesianthropus trans- Le Gros Clark WE. 1955. The os innominatum of the recent
vaalensis. Am J Phys Anthropol 7:53–77. ponginae with special reference to that of the Australopitheci-
Kimbel WH, Johansen DC, Rak Y. 1994. The first skull and other nae. Am J Phys Anthropol 13:19 –27.
new discoveries of Australopithecus afarensis at Hadar, Ethio- Le Gros Clark WE. 1964. The fossil evidence for human evolution:
pia. Nature 368:449 – 451. an introduction to the study of paleoanthropology, 2nd ed.
King JW, Brelsford JH, Tulles HS. 1969. Analysis of the pitching Chicago: University of Chicago Press.
arm of the professional baseball pitcher. Clin Orthop 67:116 – Le Gros Clark WE, Leakey LSB. 1951. The Miocene Hominoidea
123. of East Africa. Fossil mammals of Africa, no. 1. London: British
Koehl MAR. 1996. When does morphology matter? Annu Rev Ecol Museum of Natural History.
Syst 27:501–542. Le Gros Clark WE, Thomas DP. 1951. Associated jaws and limb
Kramer PA. 1999. Modeling the locomotor energetics of extinct bones of Limnopitheucs macinnesi. Foss Mamm Afr 3:1–27.
hominids. J Exp Biol 202:2807–2818. Leroi AM, Rose MR, Lauder GV. 1994. What does the compara-
Kramer PA, Eck GG. 2000. Locomotor energetics and leg length tive method reveal about adaptation? Am Nat 143:381– 402.
in hominid bipedality. J Hum Evol 38:651– 666. Leutenegger W, Kelly JT. 1977. Relationship of sexual dimor-
Lague MR, Jungers WL. 1996. Morphometric variation in Plio- phism in canine size and body size to social, behavioral, and
Pleistocene hominid distal humeri. Am J Phys Anthropol 101: ecological correlates in anthropoid primates. Primates 18:117–
401– 427. 136.
Larson A, Losos JB. 1996. Phylogenetic systematics of adapta- Lieberman DE. 1997. Making behavioral and phylogenetic infer-
tion. In: Rose MR, Lauder GV, editors. Adaptation. San Diego: ences from hominid fossils: considering the developmental in-
Academic Press. p 187–220. fluence of mechanical forces. Annu Rev Anthropol 26:185–210.
Lieberman DE. 1999. Homology and hominid phylogeny: prob- McKee JK, Thackeray JF, Berger LR. 1995. Faunal assemblage
lems and potential solutions. Evol Anthropol 7:142–151. seriation of southern African Pliocene and Pleistocene fossil
Lieberman DE, Pearson OJ. 2001. Trade-off between modeling deposits. Am J Phys Anthropol 96:235–250.
and remodeling responses to loading in the mammalian limb. Mednick LW. 1955. The evolution of the human ilium. Am J Phys
Bull Mus Comp Zool 156:269 –282. Anthropol 13:203–216.
Lockwood CA, Kimbel WH, Johanson DC. 2001. Temporal trends Moyà-Solà S, Köhler M. 1996. A Dryopithecus skeleton and the
and metric variation in the mandibles and dentition of Austra- origins of great-ape locomotion. Nature 379:156 –159.
lopithecus afarensis. J Hum Evol 39:23–55. Moyà-Solà S, Köhler M, Rook L. 1999. Evidence of a hominid-like
Lovejoy CO. 1975. Biomechanical perspectives on the lower limb precision grip capability in the hand of the Miocene ape Oreo-
of early hominids. In: Tuttle RH, editor. Primate functional pithecus. Proc Natl Acad Sci USA 96:313–317.
morphology and evolution. Paris: Mouton. p 291–306. Nakatsukasa M. 1991. Monkey performance and morphology of
Lovejoy CO. 1978. A biomechanical review of the locomotor di- bones: an influence on Japanese macaque postcrania with long
versity of early hominids. In: Jolly C, editor. Early hominids of term trained bipedal walking. In: Ehara A, Kimura T, Tak-
Africa. New York: St. Martin’s Press. p 403– 429. enaka O, Iwamoto M, editors. Primatology today. Amsterdam:
Lovejoy CO. 1981. The origin of man. Science 211:341–350. Elsevier Science. p 493– 494.
Lovejoy CO. 1988. Evolution of human walking. Sci Am 259:118 – Nakatsukasa M, Yamanaka A, Kunimatsu Y, Shimizu D, Ishida
125. H. 1998. A newly discovered Kenyapithecus skeleton and its
Lovejoy CO, Heiple KG. 1970. A reconstruction of the femur of implications for the evolution for positional behavior in Mio-
Australopithecus africanus. Am J Phys Anthropol 32:33– 40. cene East African hominoids. J Hum Evol 34:657– 664.
Lovejoy CO, Heiple KG, Burstein AH. 1973. The gait of Austra- Nakatsukasa M, Kunimatsu Y, Shimizu D, Ishida H. 2000. A new
lopithecus. Am J Phys Anthropol 38:757–780. skeleton of the large hominoid from Nachola, northern Kenya.
Lovejoy CO, Cohn MJ, White TD. 1999. Morphological analysis of Am J Phys Anthropol [Suppl] 30:235.
mammalian limbs: a developmental perspective. Proc Natl Napier JR. 1959. Fossil metacarpals from Swartkrans. Fossil
Acad Sci USA 96:13247–13252. mammals of Africa, no. 17. London: British Museum of Natural
Lovejoy CO, Cohn MJ, White TD. 2000. The evolution of mamma- History.
lian morphology: a developmental perspective. In: O’Higgens P, Napier JR. 1964. The evolution of bipedal walking in the homin-
Cohn MJ, editors. Development, growth and evolution: implica- ids. Arch Biol [Suppl] 77:673–708.
tions for the study of the hominid skeleton. San Diego: Academic Napier JR. 1967. Evolutionary aspects of primate locomotion.
Press. p 41–56. Am J Phys Anthropol 27:333–342.
MacFadden BJ, Solunias N, Cerling TE. 1999. Ancient diets, Napier JR, Davis P. 1959. The forelimb skeleton and associated
ecology and extinction of 5-million-year-old horses from Flor- remains of Proconsul africanus. Foss Mamm Afr 16:1–70.
ida. Science 283:824 – 827. Newman B. 1970. Stance and gait in the flesh-eating dinosaur
Tyrannosaurus. Biol J Linnean Soc 2:119 –123.
MacLatchy LM. 1996. Another look at the australopithecine hip.
Nitecki MW, editor. 1990. Evolutionary innovations. Chicago:
J Hum Evol 31:455– 476.
University of Chicago Press.
MacLatchy LM, Gebo D, Kityo R, Pilbeam D. 2000. Postcranial
O’Higgens P, Cohn MJ, editors. 2000. Development, growth and
functional morphology of Morotopithecus bishopi, with implica-
evolution: implications for the study of the hominid skeleton.
tions for the evolution of modern ape locomotion. J Hum Evol
San Diego: Academic Press.
39:159 –183.
Ohman JC. 1986. The first rib of hominoids. Am J Phys Anthropol
Madar S. 1994. Humeral shaft morphology of Sivapithecus. Am J
70:209 –230.
Phys Anthropol [Suppl] 20:140.
Ohman JC, Lovejoy CO. 2001. The shape of a long bone’s shaft:
Martin R, Saller K. 1959. Lehrbuch der Anthropologie, Volume 2. bending stress or growth plate form? Am J Phys Anthropol
Stuttgart: Gustav Fischer. [Suppl] 32:115.
Martin RB, Burr DB, Sharkey NA. 1998. Skeletal tissue mechan- Ohman JC, Krochta TJ, Lovejoy CO, Mensforth RP, Latimer B.
ics. New York: Springer-Verlag. 1997. Cortical bone distribution in the femoral neck of homi-
Marzke MW. 1983. Joint functions and grips of the Australopithe- noids: implications for the locomotion of Australopithecus afa-
cus afarensis hand, with special reference to the region of the rensis. Am J Phys Anthropol 104:117–131.
capitate. J Hum Evol 12:197–211. Osborn H. 1906. Tyrannosaurus, Upper Cretaceous carnivorous
Maynard Smith J, Burian R, Kauffman S, Alberch P, Campbell J, dinosaur. Am Mus Nat Hist Bull 22:281–296.
Goodwin N, Lande R, Raup D, Wolpert L. 1985. Developmental Paciulli LM. 1995. Ontogeny of phalangeal curvature and posi-
constraints and evolution. Q Rev Biol 60:265–287. tional behavior in chimpanzees. Am J Phys Anthropol [Suppl]
Mayr E. 1983. How to carry out the adaptationist programme? 20:165.
Am Nat 121:324 –334. Patteson B, Howells WW. 1967. Hominid humeral fragment from
McHenry HM. 1975. A new pelvic fragment from Swartkrans and the early Pleistocene of Northwestern Kenya. Science 156:64 –
the relationship between the robust and gracile australo- 66.
pithecines. Am J Phys Anthropol 43:245–262. Paul G. 1988. Predatory dinosaurs of the world. New York: Simon
McHenry HM. 1976. Analysis of an early hominid ulna from the and Schuster.
Omo Basin, Ethiopia. Am J Phys Anthropol 44:295–304. Pieper HG. 1988. Humeral torsion in the throwing arm of hand-
McHenry HM. 1991. Sexual dimorphism in Australopithecus afa- ball players. Am J Sports Med 26:247–253.
rensis. J Hum Evol 20:21–32. Pilbeam D, Rose MD, Barry JC, Shah SMI. 1990. New Sivapithe-
McHenry HM. 1992. Body size and proportions in early hominids. cus humeri from Pakistan and the relationship of Sivapithecus
Am J Phys Anthropol 87:407– 431. and Pongo. Nature 348:237–239.
McHenry HM, Corruccini RS, Ciochon RL, editors. 1994. Early Plavcan JM. 2000. Inferring social behavior from sexual dimor-
hominid postcrania: phylogeny and function. In: Integrative phism in the fossil record. J Hum Evol 39:327–344.
paths to the past: paleoanthropological advances in honor of F. Plavcan JM. 2001. Sexual dimorphism in primate evolution. Yrbk
Clark Howell. Englewood Cliffs: Prentice Hall. p 251–268. Phys Anthropol 44:25–53.
McHenry HM, Berger LR. 1998. Body proportions in Australo- Preuschoft H, Witte H. 1991. Biomechanical reasons for the evo-
pithecus afarensis and A. africanus and the origin of the genus lution of hominid body shape. In: Senut B, Coppens Y, editors.
Homo. J Hum Evol 35:1–22. Origine(s) de la bipédie chez les Hominidés. Paris: CNRS.
McHenry HM, Temerin LA. 1979. The evolution of hominid bipe- p 59 –77.
dalism: evidence from the fossil record. Yrbk Phys Anthropol Prost JH. 1980. Origin of bipedalism. Am J Phys Anthropol 52:
22:105–131. 175–189.
McKee JK. 1993. Faunal dating of the Taung hominid fossil Rak Y. 1991. Lucy’s pelvic anatomy: its role in bipedal gait. J
deposit. J Hum Evol 25:363–376. Hum Evol 20:283–290.
Richmond BG. 1998. Ontogeny and biomechanics of phalangeal Schmid P. 1983. Ein Rekonstruction des Skelettes von A.L. 288-1
form in primates. Ph.D. dissertation, State University of New (Hadar) und deren Konsequenzen. Folia Primatol (Basel) 40:
York, Stony Brook. 283–306.
Richmond BG, Strait DS. 2000. Evidence that humans evolved Schmitt D, Stern JT, Larson SG. 1996. Compliant gait in hu-
from a knuckle-walking ancestor. Nature 404:382–385. mans: implications for substrate reaction forces during austra-
Richmond BG, Begun DR, Strait DS. 2001. Origin of human lopithecine bipedalism. Am J Phys Anthropol [Suppl] 22:209.
bipedalism: the knuckle-walking hypothesis revisited. Yrbk Schmitt D, Lemelin P, Trueblood AC. 1999. Shock wave trans-
Phys Anthropol 44:70 –105. mission through the human body during normal and compliant
Ricklan DE. 1987. Functional anatomy of the hand of Australo- walking. Am J Phys Anthropol [Suppl] 28:243–244.
pithecus africanus. J Hum Evol 16:643– 664. Senut B. 1978. Etude comparative des piliers de la palette humé-
Robinson JT. 1970. Two new early hominid vertebrae from Swart- rale. Cah Paleontol 3:1– 8.
krans. Nature 225:1217. Senut B. 1980. New data on the humerus and its joints in Plio-
Robinson JT. 1972. Early hominid posture and locomotion. Chi- Pleistocene hominids. Coll Anthropol 1:87–93.
cago: University of Chicago Press. Senut B. 1996. Pliocene hominid systematics and phylogeny. S
Rose MD. 1984. A hominine hip bone, KNM-ER 3228, from East Afr J Sci 92:165–166.
Lake Turkana, Kenya. Am J Phys Anthropol 63:371–378. Senut B. 1999. Les humains les plus anciens. Les origins de
Rose MD. 1986. Further hominoid postcranial specimens from l’humanité dossier. Hors-Série Janvier: 66 – 69.
the late Miocene Nagri Formation of Pakistan. J Hum Evol Senut B, Tardieu C. 1985. Functional aspects of Plio-Pleistocene
15:333–367. hominid limb bones: implications for taxonomy and phylogeny.
Rose MD. 1991. The process of bipedalization in hominids. In: In: Delson E, editor. Ancestors: the hard evidence. New York:
Senut B, Coppens Y, editors. Origine(s) de la bipédie chez les Alan R. Liss. p 193–201.
Hominidés. Paris: CNRS. p 37– 48. Senut B, Pickford M, Gommery D, Mein P, Cheboi K, Coppens Y.
Rose MD. 1997. Functional and phylogenetic features of the fore- 2001. First hominid from the Miocene (Lukeino Formation,
limb in Miocene hominoids. In: Begun DR, Ward CV, Rose MD, Kenya). C R Acad Sci Paris 332:137–144.
editors. Function, phylogeny, and fossils: Miocene Hominoid Simpson GG. 1953. The major features of evolution. New York:
evolution and adaptations. New York: Plenum Press. p 79 –100. Columbia University Press.
Rose MD, Nakano Y, Ishida H. 1996a. Kenyapithecus postcranial Skerry T. 2000. Biomechanical influences on skeletal growth and
specimens from Nachola, Kenya. Afr Stud Monogr [Suppl] 24: development. in: O’Higgens P, Cohn MJ, editors. 2000. Devel-
3–56. opment, growth and evolution: implications for the study of the
Rose MR, Lauder GV, editors. 1996b. Adaptation. New York: hominid skeleton. San Diego: Academic Press. p 29 – 40.
Academic Press. Spoor CF, Sondaar PY, Hussain ST. 1991. A new hominoid
Rosenberger AL, Kinzey WG. 1976. Functional patterns of molar hamate and first metacarpal from the late Miocene Nagri For-
mation of Pakistan. J Hum Evol 21:413– 424.
occlusion in platyrrhine primates. Am J Phys Anthropol 45:
Stanford CB. 2001. The ape’s gift: meat-eating, meat-sharing,
and human evolution. In: de Waal FBM, editor. Tree of origin:
Rubin CT. 1984. Skeletal strain and the functional significance of
what primate behavior can tell us about human social evolu-
bone architecture. Calcif Tissue Int 36:11–18.
tion. Cambridge, MA: Harvard University Press. p 95–119.
Ruff CB. 1992. Biomechanical analyses of archaeological human
Stern JT. 1999. The cost of bent-knee, bent-hip bipedal gait: a
skeletal samples: skeletal biology of past peoples: research
reply to Crompton et al. J Hum Evol 36:567–570.
methods. New York: Wiley-Liss, Inc. p 37–58.
Stern JT. 2000. Climbing to the top: a personal memoir of Aus-
Ruff CB. 1998. Evolution of the hominid hip. In: Strasser E,
tralopithecus afarensis. Evol Anthropol 9:113–133.
Fleagle J, Rosenberger AL, McHenry HM, editors. Primate Stern JT, Susman RL. 1981. Electromyography of the gluteal
locomotion: recent advances. New York: Plenum Press. p 449 – muscles in Hylobates, Pongo, and Pan: implications for the
469. evolution of hominid bipedality. Am J Phys Anthropol 55:153–
Ruff CB. 2000. Biomechanical analyses of archaeological human 166.
skeletons. In: Katzenberg A, Saunders SR, editors. Biological Stern JT, Susman RL. 1983. The locomotor anatomy of Austra-
anthropology of the human skeleton. New York: Alan R. Liss. lopithecus afarensis. Am J Phys Anthropol 60:279 –317.
p 71–102. Stern JT, Susman RL. 1991. “Total morphological pattern” versus
Ruff CB, Trinkaus E, Walker A, Larson CS. 1993. Postcranial the “magic trait:” conflicting approaches to the study of early
robusticity in Homo I: temporal trends and mechanical inter- hominid bipedalism. In: Senut B, Coppens Y, editors. Origine(s)
pretation. Am J Phys Anthropol 91:21–53. de la bipédie chez les Hominidés. Paris: CNRS. p 99 –112.
Ruff CB, Walker A, Trinkaus E. 1994. Postcranial robusticity in Strait SG. 1993a. Molar morphology and food texture among
Homo III: ontogeny. Am J Phys Anthropol 93:35–54. small-bodied insectivorous mammals. J Mammal 74:391– 402.
Ruff CB, McHenry HM, Thackeray JF. 1999. Cross-sectional mor- Strait SG. 1993b. Differences in occlusal morphology and molar
phology of the SK 82 and 97 proximal femora. Am J Phys size in frugivores and faunivores. J Hum Evol 25:471– 484.
Anthropol 109:509 –522. Straus WL. 1948. The humerus of Paranthropus robustus. Am J
Ruvolo M. 1997. Molecular phylogeny of the hominoids: infer- Phys Anthropol 6:285–311.
ences from multiple independent DNA sequence data sets. Mol Susman RL. 1988. Hand of Paranthropus robustus from Member
Biol Evol 14:248 –265. 1, Swartkrans: fossil evidence for tool behavior. Science 240:
Sanders WJ, Bodenbender BE. 1994. Morphometric analysis of 781–784.
lumbar vertebra UMP 67-28: implications for spinal function Susman RL. 1989. New hominid fossils from the Swartkrans
and phylogeny of the Miocene Moroto Hominoid. J Hum Evol Formation (1979 –1986 excavations): postcranial specimens.
26:203–237. Am J Phys Anthropol 79:451– 474.
Sarmiento EE. 1985. Functional differences in the skeleton of Susman RL, Stern JT. 1991. Locomotor behavior of early homin-
wild and captive orangutans and their adaptive significance. ids: epistemology and fossil evidence. In: Senut B, Coppens Y,
Ph.D. dissertation, New York University, New York. editors. Origine(s) de la bipédie chez les Hominidés. Paris:
Sarmiento EE. 1987. The phylogenetic position of Oreopithecus CNRS. p 121–132.
and its significance in the origin of the Hominoidea. Am Mus Susman RL, Stern JT, Jungers WL. 1984. Arboreality and bipe-
Nov 2881:1– 44. dality in the Hadar hominids. Folia Primatol (Basel) 43:113–
Sarmiento EE. 1994. Terrestrial traits in the hands and feet of 156.
gorillas. Am Mus Nov 3091:1–56. Susman RL, de Ruiter D, Brain CK. 2001. Recently identified
Sarmiento EE. 1998. Generalized quadrupeds, committed bipeds postcranial specimens of Paranthropus and early Homo from
and the shift to open habitats: an evolutionary model of homi- Swartkrans Cave, South Africa. Am J Phys Anthropol 41:607–
nid divergence. Am Mus Nov 3250:1–78. 630.
Tague RG. 1997. Variability of a vestigial structure: first meta- Van Valkenburgh B. 1994. Ecomorphological analysis of fossil
carpal in Colobus guereza and Ateles geoffroyi. Evolution 51: vertebrates and their paleocommunities. In: Wainwright PC,
595– 605. Reilly SM, editors. Ecological morphology: integrative organis-
Tague RG. 2002. Variability of metapodials in primates with mal biology. Chicago: University of Chicago Press. p 140 –166.
rudimentary digits: Ateles geoffroyi, Colobus guereza, and Pe- Wake DB. 1982. Functional and evolutionary morphology. Per-
rodicticus potto. Am J Phys Anthropol 117:195–208. spect Biol Med 25:603– 620.
Tague RG, Lovejoy CO. 1986. The obstetric pelvis of A.L. 288-1 Walker A, Leakey, RE. 1993. The postcranial bones. In: Walker A,
(Lucy). J Hum Evol 15:237–255. Leakey RE, editors. The Nariokotome Homo erectus skeleton.
Taieb M, Johanson DC, Coppens Y, Bonnefille R, Kalb J. 1974. Cambridge, MA: Harvard University Press. p 95–160.
Découverte d’hominidés dans le séries Plio-Pleistocénes Walker A, Pickford M. 1983. New postcranial fossils of Proconsul
d’Hadar (Bassin de l’Awash; Afar, Ethiopia). C R Acad Sci Paris africanus and Proconsul nyanzae. In: Ciochon RL, Corruccini
279:735–738. RS, editors. New interpretations of ape and human ancestry.
Taieb MM, Johanson DC, Coppens Y. 1975. Expedition interna- New York: Plenum Press. p 325–351.
tionale de l’Afar, Ethiopie (3 Campagne 1974); découverte Walker A, Rose MD. 1968. Fossil hominoid vertebra from the
d’hominidés dans le séries Plio-Pleistocénes d’Hadar. C R Acad Miocene of Uganda. Nature 217:980 –981.
Sci Paris 281:1297–1300. Walker A, Teaford MF. 1988. The Kaswanga Primate Site: and
Tardieu C. 1979. Aspects bioméchaniques de l’articulation du early Miocene hominoid site on Rusinga Island, Kenya. J Hum
Evol 17:539 –544.
genou chez les primates. Bull Soc Anat Paris 4:66 – 86.
Walter RC. 1994. Age of Lucy and the first family: single-crystal
Tardieu C. 1981. Morpho-functional analysis of the articular sur- 40
Ar/39Ar dating of the Denen Dora and lower Kada Hadar
faces of the knee-joint in primates. In: Chiarelli B, Corruccini
members of the Hadar formation, Ethiopia. Geology 22:6 –10.
RD, editors. Primate evolutionary biology. Berlin: Springer
Ward CV. 1991. The functional anatomy of the lower back and
Verlag. p 68 – 80. pelvis of the Miocene Hominoid Proconsul nyanzae from the
Tardieu C. 1986a. The knee joint in three hominoid primates: Miocene of Mfangano Island, Kenya. Ph.D. dissertation, Johns
application to Plio-Pleistocene hominids and evolutionary im- Hopkins University.
plications. In: Taub DM, King TA, editors. Current perspectives Ward CV. 1993. Torso morphology and locomotion in Proconsul
in primate biology. New York: Van Norstrand Reinhold. p 182– nyanzae. Am J Phys Anthropol 92:291–328.
192. Ward CV. 1997. Functional anatomy and phyletic implications of
Tardieu C. 1986b. Evolution of the knee intra-articular menisci in the hominoid trunk and hindlimb. In: Begun DR, Ward CV,
primates and some hominids. In: Else JG, Lee PC, editors. Rose MD, editors. Function, phylogeny, and fossils: Miocene
Primate evolution. Cambridge: Cambridge University Press. Hominoid evolution and adaptations. New York: Plenum Press.
p 183–190. p 101–130.
Tardieu C. 1991. Etude comparative des déplacements du centre Ward CV, Latimer B. 1991. The vertebral column of Australo-
de gravité du corps pendant la marche par une nouvelle méth- pithecus. Am J Phys Anthropol [Suppl] 12:180.
ode d’analyse tridimensionnelle. Mise à l’épreuve d’une hy- Ward CV, Walker A, Teaford MF, Odhiambo I. 1993. A partial
pothèse évolutive. In: Senut B, Coppens Y, editors. Origine(s) skeleton of Proconsul nyanzae from Mfangano Island, Kenya.
de la bipédie chez les Hominidés. Paris: Editions du CNRS. p Am J Phys Anthropol 90:77–111.
49 –58. Ward CV, Begun DR, Rose MD. 1997. Function and phylogeny in
Tardieu C. 1998. Short adolescence in early hominids: infantile Miocene hominoids. In: Begun DR, Ward CV, Rose MD, editors.
and adolescent growth of the human femur. Am J Phys An- Function, phylogeny, and fossils: Miocene Hominoid evolution
thropol 107:163–178. and adaptations. New York: Plenum Press. p 1–12.
Tardieu C. 1999. Ontogeny and phylogeny of femoro-tibial char- Ward CV, Walker A, Leakey MG. 1999a. The new hominid spe-
acters in humans and hominid fossils: functional influence and cies Australopithecus anamensis. Evol Anthropol 7:197–205.
genetic determinism. Am J Phys Anthropol 110:365–377. Ward CV, Leakey MG, Brown B, Harris J, Walker A. 1999b.
Tardieu C, Preuschoft H. 1996. Ontogeny of the knee joint in South Turkwel: a new Pliocene hominid site in Kenya. J Hum
humans, great apes and fossil hominids: pelvi-femoral relation- Evol 36:69-95.
ships during postnatal growth in humans. Folia Primatol Ward CV, Leakey MD, Walker A. 2001. Morphology of Australo-
(Basel) 66:68 – 81. pithecus anamensis from Kanapoi and Allia Bay, Kenya. J Hum
Tardieu C, Trinkaus E. 1994. The early ontogeny of the human Evol 41:255–368.
femoral bicondylar angle. Am J Phys Anthropol 95:183–195. Ward CV, Kimbel WK, Johanson DC. In preparation. New post-
Teaford MF. 1988. A review of dental microwear and diet in cranial fossils attributed to Australopithecus afarensis from
modern mammals. Scan Microsc 2:1149 –1166. Hadar, Ethiopia.
Teaford MF. 1994. Dental microwear and dental function. Evol Ward S. 1997. The taxonomy and phylogenetic relationships of
Sivapithecus revisited. In: Begun DR, Ward CV, Rose MD,
Anthropol 3:17–30.
editors. Function, phylogeny, and fossils: Miocene Hominoid
Teaford MF. 2000. Primate dental functional morphology revis-
evolution and adaptations. New York: Plenum Press. p 269 –
ited. In: Teaford MF, Smith MM, Ferguson MWJ, editors. De-
velopment, function and evolution of teeth. Cambridge: Cam-
Weishampel DB. 1995. Fossils, function and phylogeny. In: Tho-
bridge University Press. p 290 –304. mason JJ, editor. Functional morphology in vertebrate paleon-
Teaford MF, Ungar PS. 2000. Diet and the evolution of the ear- tology. Cambridge: Cambridge University Press. p 34 –54.
liest human ancestors. Proc Natl Acad Sci USA 97:13506 – White TD. 1980. Evolutionary implications of Pliocene hominid
13511. footprints. Science 208:175–176.
Thewissen JGM, Hussain ST, Arif M. 1994. Fossil evidence for White TD. 1994. Ape and hominid limb length. Nature 369:194.
the origin of aquatic locomotion in archaeocete whales. Science White TD, Suwa G. 1987. Hominid footprints at Laetoli: facts and
263:210 –212. interpretations. Am J Phys Anthropol 72:485–514.
Thomason JJ, editor. 1995. Functional morphology in vertebrate White TD, Suwa G, Hart WK, Walter RC, WoldeGabriel G, De
paleontology. Cambridge: Cambridge University Press. Heinzelin J, Clark JD, Asfaw B, Vrba E. 1993. New discoveries
Trinkaus E, Churchill SE, Vilemeur I, Riley KG, Heller JA, Ruff of Australopithecus at Maka in Ethiopia. Nature 366:261–265.
CB. 1991. Robusticity versus shape: the functional interpreta- White TD, Suwa G, Asfaw B. 1994. Australopithecus ramidus, a
tion of Neandertal appendicular morphology. J Anthropol Soc new species of early hominid from Aramis, Ethiopia. Nature
Nippon 99:257–278. 371:306 –312.
Trinkaus E, Churchill SE, Ruff CB. 1994. Postcranial robusticity White TD, Suwa G, Asfaw B. 1995. Corrigendum. Nature 375:88.
in Homo II: humeral bilateral asymmetry and bone plasticity. Witmer LM. 1995. The extant phylogenetic bracket and the im-
Am J Phys Anthropol 93:1–34. portance of reconstructing sort tissues in fossils. In: Thomason
JJ, editor. Functional morphology in vertebrate paleontology. Wrangham RW. 1980. An ecological model of female-bonded pri-
Cambridge: Cambridge University Press. p 19 –33. mate groups. Behaviour 75:262–300.
Witmer LM. 1997. The evolution of the antorbital cavity of archo- Wrangham RW. 1999. Evolution of coalitionary killing. Yrbk
saurs: a study in soft-tissue reconstruction in the fossil record Phys Anthropol 42:1–30.
with an analysis of the function of pneumaticity. J Vert Pale- Zelditch ML. 1987. Evaluating models of developmental integra-
ontol Mem 3 17:1–73. tion in the laboratory rat using confirmatory factor analysis.
Wolpert L. 1983. Constance and change in the development and Sys Zool 36:368 –380.
evolution of pattern. In: Goodwin BC, Holder N, Wylie CC, Zelditch ML. 1988. Ontogenetic variation in patterns of phe-
editors. Development and evolution. Cambridge: Cambridge notypic integration in the laboratory rat. Evolution 42:28 –
University Press. p 47–57. 41.
Wolpoff MH. 1983. Lucy’s little legs. J Hum Evol 12:443– 453. Zihlman A, Cronin J, Cramer D, Sarich VM. 1978. Pygmy chim-
Wood BA, Collard M. 1999. The changing face of genus Homo. panzee as a possible prototype for the common ancestor of
Evol Anthropol 8:195–207. humans, chimpanzees and gorillas. Nature 275:744 –746.