2005 Owenj

Gait and Posture 21 (2005) 95112
Review
The natural history of human gait and posture

Part 1. Spine and pelvis
C. Owen Lovejoy
Department of Anthropology, Division of Biomedical Sciences, Matthew Ferrini Institute of Human Evolutionary Research,
Kent State University, Kent, OH 44242, USA
Abstract
The human fossil record is one of the most complete for any mammal. A basal ancestral species, Australopithecus afarensis, exhibits a
well-preserved postcranium that permits reconstruction of important events in the evolution of our locomotor skeleton. When compared with
those of living apes and modern humans, this species provides a number of insights into the origin and design of the modern human frame as
well as the selective agencies that have guided its evolution during the past three million years. Evolutionary aspects of the human spine and
pelvis are reviewed, including their impact on several clinically relevant aspects of human gait and posture.
2004 Elsevier B.V. All rights reserved.
Keywords: Primate locomotion; Scoliosis; Spondylolysis; Australopithecus; Hominid
1. Introduction
The human musculoskeletal system has been rigorously
examined for centuries, and human gait has been experimentally analyzed with an almost equal intensity [1]. Our knowledge has been amassed largely for its clinical implications,
and while an understanding of the mechanics of quiet human
walking is critical to endeavors such as implant design and
surgical intervention, it provides little information about the
manner in which natural selection molded our lower limb
during the last several million years. Bipedality is commonly
performed by a variety of primates and other mammals,
even some artiodactyls. Human ancestors, however, adopted
this odd gait as their exclusive form of locomotion, and so
extensively modified their postcranium that every transport
event, whether a simple stroll of a few yards or a desperate
flight to avoid an attacking predator, became restricted to
its use.
When and why did this transition take place? What has
been the sequence of anatomical changes during its fixation? What insights do they provide with respect to common human musculoskeletal disorders? These are questions
whose answers can supply important information to the
clinician, because the natural history of a structure affords a
unique perspective otherwise unavailable using only extant
E-mail address: olovejoy@aol.com (C.O. Lovejoy)

0966-6362/$ see front matter 2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.gaitpost.2004.01.001
anatomy and performance. Complete answers to these kinds

of questions require an examination of our fossil record.
Laboratory studies of the human frame are often not
germane to deciphering such ancient anatomical transformations. Quiet human strolling was not the primary focus
of natural selection, which assuredly acted under more extreme circumstances, when our frame was used to escape
predators, to traverse craggy terrain, or in other circumstances that produce fatigue and exhaustion. In fact, modern
human gait is paradoxical in that sensethe obvious facility and ease with which we quietly walk are a result of a
honing of locomotor skills practiced in more urgent circumstances [2]. We must therefore examine the history of
human locomotion not from a traditional clinical perspective, in which level walking in healthy individuals serves
as the standard, but from an adaptive perspective, in which
human morphology can be viewed more generally. Indeed,
unless we engage our locomotor apparatus professionally, as athletes, soldiers, or laborers in certain specialties,
the majority of us probably have spent most of our lives
never fully utilizing it in ways that governed life, death, and
successful reproduction in our ancestors.
2. Methods
Because connective tissue expression can be as enigmatic as the fossil record, specimens must be viewed as
96
C.O. Lovejoy / Gait and Posture 21 (2005) 95112
exemplars rather than as archetypes presumed to lie at

population means, and arguments based on anatomical
detail can therefore be very deceptive [3,4]. Obviously,
demonstrable variations occur in the expression of muscle and ligament attachments and in the structure of joint
surfaces. These play a key role in examining the fossil
record. However, their developmental etiology and normal
variation are paramount. A classic example from human
evolutionary studies was the belief, for some time, that absence of the intertrochanteric line on the femora of some
hominids implied a poorly developed iliofemoral ligament
(of Bigelow) [5]. In fact, the line is completely absent in
a sizable proportion of some human populations [6]. Such
absence is puzzling. Why is the line robustly expressed
in some individuals but absent in others? While the line
does not appear to be expressed prior to adulthood, it also
does not seem to become more robust with advancing
age.
A number of explanations are possiblethe most likely
derives from current research in developmental biology
connective tissue structures are now known to be specified
during pattern formation by complex positional informational fields, and subtle fluctuation in such processes almost
certainly produce variances in their adult expression [7,8].
Contrary to long-standing assumptions, it is now clear
that the robusticity and/or rugosity of entheses are very
probably not strain dependent. Rather, these are complex
structures [9,10] whose expression and migration during
growth are determined principally, if not exclusively, by
pattern formation and not by strain magnitude or frequency.
The implication is that careful inspection of an adequate
sample is therefore required to determine whether a character provides any significant information about underlying
musculoskeletal structure: it is just as important to avoid
misleading interpretation of anatomical features with such
fluctuating degree states (particularism) as it is to avoid

its parent fallacy of adaptationism [3,4].
As we have detailed elsewhere [11,12], it is now possible to construct reasonable hypotheses of the probable developmental etiology of many mammalian musculoskeletal traits. Such traits are divisible into two primary
categoriesthose which have a distinct genic basis fixed
and integrated during pattern formation and those which
are largely the product of connective tissues response to
their environment, sensu lato. In addition, because pattern formation resides in cis-regulated cellular expression
fields and modules [8,13,14], modifications of the musculoskeletal system which are true target changes can be
expected to be accompanied by associated auxiliary ones
which are merely non-selected (i.e., pleiotropic) byproducts. Expositions of the musculoskeletal systems of extinct
animals therefore require careful sifting in order to separate real targets from their companion, auxiliary effects.
Given our improved knowledge of developmental biology,
the practice of attributing functional significance to traits
that are little more than anatomical minutia is no longer
credible. We have elsewhere proposed trait categories generated from the point of view of developmental dynamics. These are reproduced for convenience in Table 1; a
more detailed exposition of their meaning may be found
elsewhere [15].
3. Evolutionary framework
The hominid fossil record is one of the most complete
for any extant mammal, and is the product of an intensive search for specimens, favorable taphonomic conditions (i.e., context of fossilization and recovery) in East,
South, and Central Africa, and target animals which were
Table 1
Analytical trait typesa
Type 1: A trait which differs in two taxa because its presence and/or expression are downstream consequences of differences in the positional
information of its cells and their resultant effects on local 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 field
deployment and the functional biology of their adult product. For example, the superoinferior shortening of the ilium in hominids.
Type 2: A trait that is a collateral byproduct of other field changes. Type 2 traits differ in two taxa because of differences in pattern formation (as in
Type 1), but have no functional consequences. Unlike Types 4 and 5, they represent true field derived pleiotropy. Type 2A traits are those whose
primary antecedent shift was the product of natural selection. Type 2B traits are those whose parent changes were not under selection. They are
likely to result from minor fluctuations in morphogenetic fields, and differences in their expression among demes arise by stochastic processes, such
as genetic drift (for examples, see text).
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.
For example, body size and its allometric effects. Allometric shifts probably usually reflect slight changes of systemic control factors during
development: e.g., small modulations of GH and/or its related factors can generate fully coordinated morphological change.
Type 4: A trait that differs between taxa because its presence/absence and/or grade are attributable exclusively to phenotypic effects of the interaction
of systematic assembly mechanisms [11] such as cartilage modeling and environmental stimuli. Such traits have no antecedent differences in
pattern formation, and therefore have no value in phyletic analysis. They are epigenetic and are not pleiotropic. However, they can provide significant
behavioral information, and are therefore of expository or evidentiary value in interpreting fossils. They result from habitual behaviors during
development. For example, the bicondylar angle of the femur.
Type 5: Traits arising by the same process as Type 4, but which have no reliable diagnostic value with respect to significant behavior. Such traits are not
consistently expressed within species and often show marked variation of expression within individuals and demes. For example, femoral anteversion.
a
For further discussion, see [11,12,15].
97
Fig. 1. Early hominid species that preserve some significant portion of the postcranium (only specimens with associated postcrania are illustrated). All
are roughly arranged according to approximate likely phylogenetic relationships. While a plethora of nomina are currently employed to reference these
species, further examination is likely to reveal that only two major phyletic lines emerged between 6 and 2 MYA. One of these led to several extinct
species of Australopithecus, while the other led to H. habilis and its eventual successor H. sapiens, via H. erectus (the latter is represented here only by
its earliest major specimen: KNM-WT15000) (L.B. Spurlock/M.A. Mcollum).
demographically successful and capable of invading new

habitats
[16,17].
While several taxonomic issues are still currently in
debate, a general picture of early hominid evolution has
emerged and is summarized in Fig. 1. Palaeogeographic
and DNA hybridization data suggest that humans shared a
last common ancestor (LCA) with the African apes (Pan
troglodytes, Pan paniscus, Gorilla gorilla) during a period
79 million years ago (MYA) [18]. There is little question
that the LCA was geographically African.
The collection of fossils from 4 to 7 MYA has recently
burgeoned. Only a few years ago, specimens were recovered from Ethiopia of such great age and primitive structure
as to justify a new genus. Designated Ardipithecus ramidus
(from the Afar language: root [ramidus] of the ground apes

[Ardipithecus]) [19], this species was first described only
for a narrow time span around 4.4 MYA, but more fragmentary remains are now known to extend it almost to 6 MYA
[20]. This makes it roughly contemporary with two recently
named taxa, Orriron tugenensis [21] and Sahelanthropus
tchadensis [22]. Neither has been described in sufficient
detail to be considered here, but upon closer examination,
both are very likely to be similar to and congeneric with
Ardipithecus.
A more recent species from Kenya is Australopithecus
anamensis [23]. It now serves as the horizon species of the
genus Australopithecus first defined in 1925 (A. africanus)
[24]. The South African cave sites in which Australopithecus
was discovered have continued to be productive and useful
98
Fig. 2. Relationship between thorax and spine in an Old World monkey (baboon: top), an African ape (gorilla: middle), and a modern human (bottom).
The architectural sketches to the left illustrate the special methods of presentation that have been used to render these transverse thoraxes/pelves sections;
viz., each has been drawn without any perspective-based size reduction (of increasingly distant elements) caused by parallax. For each specimen the
maximum point of horizontal projection of the thorax away from the vertebral column (dashed line) (T11 in the Old World monkey; T10 in the gorilla and
human) was determined with an anatomical line of sight (parallel to the vertebral column; column B). The thorax was then drawn a second time with
the line of sight being the true vertical (column A) (the position of the reference thoracic vertebrae is shown in column A, but not B). Thus if walking
upright using typical orthograde postures, the projections of the thorax in the Gorilla and OWM are most similar to their relationships in column (A)
Each specimen was drawn and metrically verified from a ligamentous thorax fixed in an orthograde posture typical of its taxon (baboon: sitting; gorilla:
climbing; human: quiet standing). Note the following: (1) the anatomical axis of the iliac crest is essentially anteroposterior in the OWM, but is distinctly
mediolateral in the two hominoids. (2) While the human and gorilla show invagination of the column into their (anteroposteriorly flattened) thoraxes (cf.
Fig. 6), the thorax still projects anteriorly in the gorilla, i.e., note the sagittal separation of T10 and S1 in the Gorilla but not the human. (3) As shown
in the examination of the human locomotor record, but they

are, for the most part, more recent than many East African
sites.
All australopithecines may now be broadly assigned to
one of two lineages which probably diverged from each
other between 3 and 2 MYA (Fig. 1). These appear to
have shared a last common ancestor in the form of Australopithecus afarensis (and by extension A. anamensis and
Ar. ramidus), which is now known from the time span of
3.72.8 MYA. It is currently the fashion to complicate these
(probably much simpler) relationships by an exuberant exploitation of anatomical detail, but most such taxonomic
fabrications are likely to evanesce as normal anatomical variation and its genic basis become more widely
appreciated.
While there are still major gaps in this record, it nevertheless provides a clear picture of the evolution of our
locomotor skeleton. Fossils assigned to Ar. ramidus have
received only taxonomic announcement and cannot yet
contribute to that picture. Femora from O. tugenensis have
been partially described and will be discussed briefly below. Postcranial specimens from A. anamensis are still rare,
and for the lower limb comprise only isolated fragments of
the tibia and foot. Conversely, remains of A. afarensis are
now abundant and include the partial skeleton from Afar
Locality (AL) 288 (Lucy). In addition, its two descendant lineages provide insight into those characters clearly
shared by common ancestry, and even though study of Ar.
ramidus and Ar. anamensis will undoubtedly enhance understanding of our evolution, more recent specimens offer
many insights into the emergence of the human frame.
Because of its pivotal position in early human evolution,
A. afarensis will therefore be the primary focus of this
presentation.
4. Spine
4.1. The lumbar spine of hominoids
Some years ago, in an especially cogent discussion of the
epaxial region of higher primates, Benton made a distinction
between short-backed and long-backed forms [25]. The
short-backed group includes hominoids and several New
World monkeys, all of which exhibit a series of complex
modifications of their forelimb and axial skeletons. While
these vary substantially, all evince a forelimb that is used
99
more extensively for suspensory locomotion than in other

higher primates, and by a substantial reduction in the length
of the lower back.
The morphological changes that permit increased suspension vary, but always include a change in thoracic (and
scapular) shape [26] and a significant reduction in the length
of the free lumbar column [27]. In the great apes, this involves a reduced lumbar number, and an immobilization of
the lowest one or two vertebrae by entrapment between
the ilia. As a result, great apes exhibit remarkably immobile
lower spines, often with the distance between their thorax
and iliac crests amounting to little more than one or two
intercostal spaces [27] (Fig. 2). These changes effect a direct attachment of the thorax to the pelvis, creating a stiff
unibody, with no flexibility of the lower back. Whether
this serves as a base of support for bridging gaps in the arboreal canopy [28], or reduces spinal injury caused by lower
limb inertia during arboreal clambering (with an enlarged
body mass) is largely irrelevant to the present discussion.
What is relevant is the central role that lower back mobility
played in the origins of habitual upright walking.
When walking bipedally chimpanzees and gorillas exhibit a bent-hip/bent-knee (BHBK) gait [29,30]. It is a
common misconception that this derives primarily from
anatomical limitations of the hip joint. To the contrary, it is
a direct consequence of an inability to position the center of
mass of the head, arms, and trunk (HAT) over the point of
ground contact without simultaneously flexing both the hip
and knee.
Walking significant distances with BHBK gait is fatiguing
because of the poor leverage at these joints when they are
used in less than full extension. Fatigue reduces the ability
to perform protective negative work, and thereby exposes
the entire lower limb to injury. The lumbar spine must therefore have been a focal point in our earliest adjustments to
habitual bipedality.
The modern human lower spine is exceedingly mobile
compared to that of the great apes (and other short-backed
primates) because it exhibits several unique anatomical
features (Figs. 25). These include greater overall length,
but especially a shortening and pronounced broadening of
the ilia and sacrum. These eliminate any restrictive contact
between the lower lumbar vertebrae and the retroauricular
portion of the ilia. Hominid lumbar vertebrae also exhibit
a caudally progressive widening of their laminae and the
space separating their articular processes (zygapophyses)
[3133].
in the left column, the combination of lumbar shortening, greater superior projection of the iliac crest (so as to shorten its distance to the most caudal
rib), and the invagination of the column into the thoracic space together have resulted in a rigid pelvic-thoracic link in hominoids. (4) However, while the
gorillas thorax is well positioned for rigidity with respect to its pelvis, it causes very large bending moments relative to the hip joints in bipedal posture.
(5) In the human, lordosis (made possible by columnar elongation) has translated the column anteriorly so that it overlies the hip joints in erect stance
(superior compensation for lordosis now places T10 lies posterior to S1) (6) The relatively great mediolateral breadth of the human sacrum compared to
the other primates. Factors 5 and 6 are the key, and therefore probably the initial, adaptations to upright walking. These relationships were fully established
in A. afarensis, but its pelvis had not yet been remodeled to assure passage of large-brained fetuses (see text) (L.B. Spurlock/M.A. McCollum).
100
Fig. 3. Size relationship between superior zygapophyses of the L3 and sacrum: (A) chimpanzee; (B) gorilla; (C) AL-288-1; (D) human. The cartoon to
the left demonstrates that the L3 in each specimen has been rotated 180 . Note that the transverse distance separating the joint facets in the African apes
is greater in L3 than in the sacrum, whereas the reverse arrangement is present in the two hominids. The latter is probably the consequence of a growth
gradient effect established by overall broadening of the sacrum (cf. Figs. 5 and 11).
It has been argued that this widening permits greater

encroachment of each pair of inferior zygapophyses onto
the cranial surface of the neural arch of the vertebrae caudad to it, thereby facilitating lordosis (Figs. 34) [34]. A
simpler explanation now seems more likely. As will be
discussed below, those modifications of the pelvis that permitted the establishment of human-like bipedality in early
hominids involved dramatic broadening of the sacrum. A
cranio-caudal pattern formation gradient, which progressively enlarged somite, condensation, or anlagen size, is
therefore the simplest and most probable explanation of this
feature (see below), because its result would have been to
assure free mobility of the lower lumbar column.
Modern humans also differ from other hominoids in the
spatial orientation of their lumbar articular facets [31,33].
Progressing caudally, human facets become more coronally
oriented, whereas those of chimpanzees become more sagit-
tally oriented. The novel orientation in humans may resist

anterior displacement of L5(6) at the L5/S1 jointa potential injury imposed by extreme lordosis (especially the
elevation of the caudal tip of the sacrum-also necessary to
potentiate a sufficient pelvic outlet for a large-brained fetus
(see below)).
4.2. The fossil record of the hominid lumbar spine
The only substantial evidence of vertebral structure in
A. afarensis is provided by a single lumbar vertebra from
AL-288-1 (probably L3) [35]. As with humans, the transverse distance separating the facet joints in AL-288-1 is
far greater in the sacrum than in the L3 (Fig. 3). As would
be expected to accompany this specialization, conspicuous
imbrication pockets are present (Fig. 4). These serve
as strong (Type 4; cf. Table 1) evidence of considerable
Fig. 4. Imbrication pockets in hominid lumbar vertebrae. Arrows on each L3 indicate the marginal limit of the area excavated by contact with the
inferior zygapophyses of L2. (A) L2/L3 from a modern human. (B) Isolated L3 of AL-288-1 (cast). For further discussion see text.
101
Fig. 5. Frontal projections of hominoid pelves. (A) chimpanzee; (B) AL-288-1; (C) human female; (D) human male. Note the dramatic shortening of
the ilia in the hominids and the absence of any dorsal projection that might entrap the last lumbar (L5 in humans; L6 in A. afarensis). Note the much
closer geometric similarity of AL-288-1 to the human male than female, despite its very large interacetabular distance (a female character in modern
humans). The human pelvis has been entirely remodeled so as to greatly enlarge its birth canal. Note the extremely broad sacra of the hominids in
comparison to the very narrow one of the ape (L.B. Spurlock).
lordotic flexibility of the lumbar column. As with modern

humans, its sacral facets have a more coronal orientation
than do those of apes (Fig. 3) [31,36].
Two early hominid lumbar spines have been recovered
for A. africanus (StS-14 [36,37] and StW-431 [38]), a descendant species of A. afarensis (Fig. 1). Both preserve a
substantial portion of the sacrum [39]. The well-preserved
lower spine of STS-14 confirms, unsurprisingly, the caudally progressive widening of the lumbar zygapophyses in
this descendant of A. afarensis. Both STS-14 and AL-288-1
preserve complete os coxae, which permit examination of
relationships between their lowest lumbar vertebrae and iliac crests (Fig. 5). Both show an absence of the restrictive
reticular relationships normally seen in African apes (i.e., iliac capture of lower lumbar vertebrae), and while the last
lumbar vertebra of STS-14 is sufficiently far recessed into
the pelvis to allow powerful ligamentous connections onto
the . . . surface of the auricular region ([37], p. 104), there
is, nevertheless, fully ample isolation sufficient to permit
marked lordosis [37].
A thorough review of the australopithecine lumbar spine
was recently conducted by Sanders [36], who notes a number of features shared by humans and australopithecines.
Whereas in non-human primates lumbar bodies are characteristically ventrally-wedged, the last four vertebrae of
STS-14 are dorsally wedged as in humans, and despite some
minor metric differences in the spatial position of their transverse processes, expansion of the postero-medial portion of
the iliac crest and strong development and dorsal reflection

of the posterior superior iliac spine . . . are all synapomorphic
[i.e., shared because they are derived after separation from
the LCA] with the condition in modern humans, indicating
that functional demands for erector spinae muscles...to resist forward flexion of the trunk were similar to those of
modern humans ([36], p. 2701). Sanders also finds that
their lumbar zygapophyses and sacral facets closely resemble those of modern humans, as do the dorsal angulations
of their lower lumbar zygapophyses.
Of special interest is the number of lumbar vertebrae in
these two specimens of A. africanus. Both probably exhibit six lumbar vertebrae, at least when they are viewed
functionally; that is, the six lowest pre-sacral vertebrae all
have lumbar-like potential movement. This almost certainly
reflects a shift in the expression boundaries of one or more
Hox genes (e.g., Hoxa9, Hoxb9, Hoxc9) relative to their expression in Homo sapiens. Whether the number of thoracic
vertebrae was also reduced to 11, or 12 thoracic vertebrae
were instead maintained and the shift was more caudal
(lumbo-sacral), or the number of presacral somites incremented, cannot be resolved because the thoracic columns
in both specimens are incomplete. In any case, however,
australopithecines had lumbar spines that were more mobile
and capable of lordosis than are those of average modern
humans.
While most observers have concluded that both STS-14
and STW-431 exhibit six lumbar vertebrae [31,36,37,39],
102
Haeusler et al. recently presented detailed arguments [40]

that these two specimens exhibit only five lumbar vertebrae
(as well as KNM-WT15000, a specimen of H. erectus also
described as having six lumbar vertebrae [31,36,41]; see below), but with the last thoracic essentially having lumbar-like
function. Their arguments are based on traditional anatomical analysis (presence/absence and location of rib facets,
etc.), and need not be considered further here. Even they
conclude that all three fossils differ from the majority of
modern humans in that it is the seventh presacral vertebra
where the orientation of the articular facets changes ([40],
p. 634), thus making lordosis possible over a longer range
of the lower back.
The implications are quite profound. Since apes exhibit
the opposite change of lumbar column reduction (Fig. 2),
the demonstrably more lordotic column in Australopithecus
than occurs even in most H. sapiens signals skeletal reorganization assuring virtually complete abandonment of arboreal activity in favor of permanently terrestrial life. That is,
if climbing induces the entire elimination of any mobility in
the lower backs in (essentially quadramanual) arboreal apes,
it is, by extension, antithetical to arboreality in a species
in which so many other critically important adaptations for
climbing had also been abandoned (see below).
4.3. Reconstructing the emergence of the early hominid
lumbar spine from the LCA
An important character that must have accompanied lumbar reduction in ancestral hominoids is a precipitous reduction in the mass and cross-sectional area of the m. erector
spinaeso much so that its ventral boundary (the transverse processes) becomes dorsally relocated to the lumbar
pedicles, rather than lying on the centra as in quadrupedal
monkeys. This serves as a morphological marker for a
short-backed primate because it is naturally coincident
with the precipitous reduction of control by a massive m.
erector spinae [25].
It is of interest in this regard that the erector spinae
are epaxial, and that the pedicle is the approximate dorsal
boundary of Pax1 expression in the developing sclerotome,
whereas the spinous processes and neural arches are modulated by Msx1 and Msx2 whose expression is ultimately
controlled (via BMP4) by the roofplate and overlying ectoderm (for details, see [42]).
Apes can only have afforded such reduction of their
erector spinae if it was simultaneously accompanied by
passive spinal immobilization so as to prevent habitual
Euler buckling of the column (that is, by virtue of the combined deformation of its individual disks), though shortening
of the column has largely eliminated this prospect in apes
[43,44]. Such changes were very likely also associated with
other modifications of the thorax (and abdomen), including an imagination of the spine ventrally into the thorax
(Fig. 6) [27], a character which increases column rigidity and which was presumably associated with their more
Fig. 6. Invagination of the vertebral column into the thorax and its effect
on both structural integrity and scapular position. (A) Old World monkey
(OWM) (macaque); (B) chimpanzee; (C) human. The primary axis of the
scapular blade in the monkey is nearly anteroposterior (its iliac crests
are also anteroposteriorly oriented (cf. Fig. 2)). In the two hominoids,
the vertebral column has become invaginated into the thorax, greatly
increasing its rigidity, and making it more elliptical. This has also caused
the scapular axis to become more mediolaterally oriented. The invagination
is more dramatic in the human because of lumbar lordosis. Thoraxes
redrawn from Schultz [27] who traced plaster casts of eviscerated thoracic
cavities.
posterolaterally repositioned shoulder girdle than occurs in

monkeys.
A lumbar vertebra recovered from the late Miocene
ape specimen (CLI-18800; Dryopithecus) exhibits a clear
pedicular origin of its transverse processes, confirming that
ape-like vertebral columns had already emerged by circa
9 MYA and would have been present in the LCA [45]
(an earlier specimen from Moroto, Uganda approximately
1520 MYA in age, also displays this advanced morphology [43]). Thus, hominids appear to have re-evolved
their free lumbar columns from a short-backed progenitor, rather than having retained the longer column of a
more generalized ancestor, as the human column, despite
103
its length, evinces clear overall short-backed morphology

(cf. Fig. 2).
4.4. Clinical implications afforded by the fossil record of
our spine: scoliosis
The above conclusion is of interest with respect to the
incidence of a modern human malady, idiopathic scoliosis.
In a recent survey of a large sample of great ape skeletons
by B.M. Latimer of the Cleveland Museum of Natural History, no cases of scoliosis were observed in several hundred
chimpanzee and gorilla spines.
Such a finding is in accord with the observations of Lowe
and colleagues [46]. Naturally occurring scoliosis in vertebrates is seen almost exclusively in humans. . . .[I]t has been
difficult to distinguish causative factors from those that may
result from the condition. . . . The current thinking is that
there is a defect of central control or processing by the central nervous system that affects a growing spine. . . and that
the spines susceptibility to deformation varies from one individual to another ([46], p. 1165). However, [a]ny hypothesis that proposes a neurological defect must account
for the impression that many patients with idiopathic scoliosis have above-average ability in sports. These observations
have been largely anecdotal, but a study of girls attending
ballet school showed that the prevalence of scoliosis may be
as high as 20 percent ([46], p. 1162).
These conclusions are fully concordant with the highly
unusual situation that characterizes modern humans, viz.,
a re-elongated lower spine with what can only be described,
compared to other primates with long lower spines, as a
semi-competent erector spinae. Significant lumbar deviation is prevented in apes by their precipitous lumbar reduction, lumbar vertebra capture by their ilia, and in Old
World monkeys by their massive erector spinae (Fig. 7).
While this may not account for idiopathic thoracic manifestations of the disorder in humans, subtle imbalances in
the elongated human lumbar spine might possibly play an
initiating role even though they would remain subclinical
until downstream and more cranial effects became more
prominent.
At a minimum lumbar scoliosis is seriously debilitating
and should have long been a target of strong selection. Why
is it still prevalent in humans? The logical response is that
selection for effective bipedality must have been so vigorous
in the ancestors of A. afarensis that functional lordosis was
facilitated despite the increased risk of scoliotic deviations
and flexion-induced injury permitted by a semi-competent
erector spinae. The functionally elongated lumbar column
of Australopithecus and its descendants must have predisposed them to even greater rates of spinal pathology than
occur in modern humans. It is important in this regard that
the spine of KNM-WT15000 H. erectus skeleton displays
substantial evidence of scoliosis, including both thoracic
asymmetry and vertebral fracture (J.C. Ohman, B.M. Latimer, personal communication; observations by the author).
Fig. 7. Hybrid comparison of the erector spinae of an OWM (Cercopithecus) (left) and a human (right) (see [25] for a similar comparison with
a chimpanzee). The two vertebrae have been scaled to the same anteroposterior overall dimension. The massive erector spinae of the monkey
carries its anterior border, its transverse process, well onto the vertebral
body; that of the human (typical of hominoids) is restricted to its pedicle, greatly reducing the muscles cross-sectional area. Loss of erector
spinae mass is largely a byproduct of thoracic rigidification caused by
a substantial anterior projection of the column (cf. Fig. 6). The loss of
the massive erector spinae in ancestral hominoids, coupled with subsequent lumbar column elongation in hominids, has resulted in superoinferior elongation of the distance between pelvis and thorax. Because it also
no longer benefits from control by a massive erector spinae ideopathic
lumbar scoliosis of the lower column is probably a malady peculiar to
hominids, and continues to be prevalent in modern humans, despite idieopathic reduction of the column from six lumbars to five over the course
of the Plio-Pleistocene. OWM erector spinae structure and size from [25];
that of humans from [80] (L.B. Spurlock).
Risk of scoliosis may have served as the most prominent selection factor favoring reduction in the length of the human
lumbar column over the course of the Plio-Pleistocene.
4.5. Clinical implications afforded by the fossil record of
our spine: spondylolysis
Also of some clinical interest is Latimers recent review
of spinal morphology associated with spondylolysis, another
malady which does not occur in apes, but which is common
in humans (about 5% of the population [47]). Latimer has
argued that spondylolysis is more frequent in individuals in
which the inferiorly progressive spread of the lowest lumbar vertebra is less than those of normal, non-spondylolytic,
spines, suggesting that the disorder is epigenetic and may
derive from excessive propinquity of the neural arches during the initial lordosis of early childhood bipedality.
Any debilitating effects of spondylolysis (i.e., spondylolesthesis) have apparently either occurred only sporadically,
or without sufficient frequency during middle-adulthood
(most individuals in earlier human populations rarely survived to more than 45 years) to have had little selective
effect. That is, whatever its cause, spondylolysis has not
been eliminated by selection over the past 34 MY.
104
Furthermore, the argument that it is caused primarily by

an insufficient progressive spread of the lumbar zygapophyses inferiorly [31,34] is probably also now null. If this were
its primary cause, and the progressive spread its primary
remedy, why would selection have not already eliminated the
condition? It would now appear far more likely that, as noted
earlier, this special lumbar character in hominids is simply
a product of a developmental size gradient that guarantees
spatial separation of the lowest lumbar vertebrae from the
(posterior superior iliac spines) PSISs of the ilia, thus assuring maximum potential lordosis. Spondylolysis has probably
increased by virtue of lumbar count reduction (thus increasing the lordotic angle at each joint), but since spondylolesthesis is much later in onset, it is possible that selection has
favored reduction in the incidence of scoliosis by reducing
lumbar column length despite the latters unfavorable effect
on spondylolysis.
5. Pelvis
The ability to fully extend the hip and knee made possible
by lower spinal retroflexion (lordosis) would have greatly
reduced fatigue during extended bouts of upright walking,
but ultimately such fatigue could only have been fully eliminated by a reorganization of pelvic muscle function. In the
shift from quadrupedal progression to bipedality the activity
of the hamstrings becomes primarily restricted to the control and deceleration of the limb in the final stages of swing
phase (along with a variety of other postural duties) and
the mm. gluteus minimus and medius to pelvic stabilization
during single support. The m. gluteus maximus becomes the
principal stabilizer of the trunk upon the lower limb, bracing the sacroiliac joint (and protecting it by eccentric contraction), and controlling forward rotation of the trunk at
ground contact [34,48,49]. The quadriceps, along with the
plantarflexors (with which their contraction must be synchronized), become the primary muscles of propulsion by
extending the knee with the limb fixed against the substrate.
5.1. The fossil record of the hominid pelvis
Two Australopithecus specimens exhibit virtually complete innominates. These have required some significant
restoration (AL-288-1) [50,51] or reconstruction (STS-14)
[52], but the former is so complete that given bilateral symmetry, it can be regarded as an intact pelvis. However, because it was found in a crushed state in which its posterior
iliac crest had been bent 90 out of position (Fig. 8 [51]), any
deliberations absent repair of this global deformation (see,
for example [5357]) are irrelevant to the current discussion.
That the primary shifts necessary in the pelvic platform
to effect all of the fundamental changes in muscle function
seen in modern humans were also fully accomplished in
A. afarensis can be gleaned from study of various dimensions and morphological characters of AL-288-1. The novel
Fig. 8. Superior view of iliac crest of the left innominate of AL-288-1

(original specimen). While much of the iliac blade is well preserved,
the posterior third has been crushed, crumpled, and bent anterolaterally
almost exactly 90o (PSIS: posterior superior iliac spine). Since the dislodged portion includes the auricular surface, the anatomical structure and
relations of the pelvis cannot be determined prior to restoration; indeed, if
the sacrum and unrestored innominate are articulated and mirror-imaged,
a gap of several centimeters occurs at the pubic symphysis. Therefore,
analyses of the hip joint of A. afarensis that are based upon its unrestored
condition must be disregarded in discussions of its locomotor behavior.
locomotor-related aspects of the human pelvis are present,

and coupled with the introduction of lordosis, signal a fully
human-like posture and gait.
Of particular importance is the mosaic nature of the
AL-288-1 pelvis, with its ilium and superior portion having
been dramatically broadened and reduced in height, but
with the lower pelvis (pubis and ischium) still retaining
some aspects of its LCA heritage. In modern humans, an
approximate postural plane can be defined (viewed in lateral perspective, Fig. 9) by a vertical line drawn tangential
to its anterior superior iliac spines (ASISs) and pubic tubercles. This is not the case with AL-288-1, which clearly
retained a more primitive position of its pubic corpora,
105
Fig. 9. Lateral views of pelves shown in Fig. 5 with sacrum outlined for visibility. While the upper pelvis of AL-288-1 is quite similar to the two human
ones in this projection, its superior pubic ramus is still inferiorly directed as in the chimpanzee. In this species this negates use of the rule of thumb
which orients a human pelvis close to anatomical position when the ASIS and pubic tubercle are placed in the same vertical plane. However, sacral
lordosis and the line of action and disposition of the anterior gluteals are virtually identical in AL-288-1 and modern humans. The elevation and anterior
projection of the superior pubic ramus in humans are a consequence of the substantial increase in the anteroposterior dimension of the birth canal, and
the need to raise the pubis so as to establish a shorter cylinder to permit asynclitism to have its beneficial effects during parturition. These changes are
unrelated to locomotion. Note the human-like faceted disposition of the origins of the hamstrings in AL-288-1, unlike the single plane present in the
chimpanzee tuberosity (L.B. Spurlock).
which are both sagittally short (though they are markedly

long mediolaterally, see below) and inferiorly deflected like
those of a chimpanzee (Fig. 9); that is, the rule of thumb
used to spatially orient a human pelvis cannot be applied
to AL-288-1 because of the conserved structure of its anterior lower pelvis. These lower pelvic differences between
humans and A. afarensis are a consequence of the formers
greatly expanded birth canal (see below and the legend of
Fig. 10 for these birth-related features).
The iliac changes in AL-288-1 have completely altered
its structure from that of its African ape relatives, and as
noted earlier, this change in shape has almost certainly been

brought about by both a change in the form of its anlagen
(and presumably its antecedent condensation), as well as
growth patterns. This wholesale modification of developmental patterning is attested to by the presence of a large
Anterior Inferior Iliac Spine (AIIS) whose size and proportion virtually guarantee that it arose in AL-288-1 via a novel
growth plate and apophysis (other primates lack a secondary
center of ossification for the AIIS). The broadened, lowered,
and laterally flared ilium in A. afarensis placed the anterior
abductors in a position for active pelvic management of
106
Fig. 10. Mechanisms of birth in the chimpanzee (left), AL-288-1 (center), and modern human (right). Cephalo-pelvic relationships are shown for the inlet
(top), midplane (center), and outlet (bottom). Vault sutures are indicated by dotted lines to show orientation of the fetal cranium. Note that in the human
the anterior fontanelle is not visible in the midplane because of cranial flexion, but reappears in the outlet view as the cranium begins its extension. Birth
in AL-288-1 was probably simple, inasmuch as the term fetal cranium was probably of the same approximate size as that of a chimpanzee, and because
no reorientation in any of the three stations was required, save for rotation at entrance into the inlet as in humans (but with no further reorientation) [61].
single support phasei.e., one from which they could

abduct at or near their resting length, thus minimizing fatigue. This unique capacity of the hominid hip to prevent
pelvic drop (Trendelenburgs sign) during single support has also gained significant mechanical advantage in
AL-288-1 by virtue of its extraordinarily long femoral neck.
Indeed, neck length in number of isolated proximal femoral
specimens of Australopithecus exceeds that of any other
primate including modern humans.
The hip of Australopithecus is thus not intermediate between apes and humans but is instead a unique mosaic,
which combined changes of the upper pelvis that facilitated bipedality with a more primitive lower pelvis not yet
modified to encourage passage of a massively brained fetus. Its elongated femoral neck, moreover, is accompanied
by another unique feature of the pelvis in A. afarensisa
relatively broad interacetabular distance (Fig. 5). The combination of these anatomical features results in abductor
lever arm ratios that are roughly similar to those of modern humans. Why did australopithecines exhibit such long
interacetabular distances?
5.2. The early hominid pelvis was adapted to bipedality
but not to the parturition of large brained infants
A variety of unusually inventive suggestions has been
offered to account for this specialized morphology (see,
for example [58,59]). These have centered around the presumption that wide separation of the hips slightly increased
stride length (why the much simpler and direct change of
merely increasing lower limb length was not adopted is
left undiscussed). Such suggestions suffer from the uncritical practice of using modern humans as a comparative
standard against which to measure the degree to which
other hominids were incompletely adapted to bipedality.
Assigning function to every anatomical detail that differs
from the modern human condition represents a failure to
analyze intermediate forms dynamicallythat is, to consider the manner in which anatomical form is altered via
changes in the morphogenetic process, rather than its adult
end-products. Such deficiencies in approach invariably result
in assigning dissimilarities of australopithecines and humans
to some degree of functional intermediacy of the former
(see earlier).
Modern humans, however, are not simply bipeds: they
are bipeds with relatively enormous brains. As such, successful parturition is an even more powerful selective force
than locomotor pattern: its effects on reproductive success
are immediate and profound. Humans have evolved largely
circular pelvic midplanes (i.e., the greatest area is provided by a constant radius), with any deviation from this
form being proportionately disadvantageous [60]. Selection
has therefore only managed to produce a marginally satisfactory birth canal by modifying pelvic form in order to
accentuate the area of the midplaneits original australopithecine form was wholly inadequate by modern standards.
The very broad interacetabular dimension of australopithecines would have provided no particular benefit for
birthing, as it greatly exceeds the more critical anteroposterior diameter of the pelvic ring in these early hominids
[61]. Given that their pelves give no indication whatsoever of being locomotorly intermediate with humans
(see above) nor as strongly challenged obstetrically, the
answer to this problem therefore lies in the nature of the
genetic/evolutionary process by which their complex morphological changes were achieved from the LCA.
We will turn to this point directly, but at this point it
must be emphasized once again that those morphological
changes that were effected between A. afarensis and H. sapiens cannot have reflected improved mechanics: had the long
femoral neck and pronounced lateral iliac flare been retained
in the descendants of A. afarensis (along with a reduction in
only the relative interacetabular distance in the pelvis), the
mechanical advantage to the abductors in modern humans
would now be far greater than it actually isthe reduction
of these mechanical benefits must thereby have been part of
the pattern formation shifts required to increase the dimensions of the birth canal and not a response to any change in
gait pattern.
5.3. Reconstructing the emergence of the early hominid
pelvis from the LCA
The early hominid pelvis had to be anatomically modified
from a more primitive ancestral one and, as noted earlier,
changes in the upper pelvis clearly antedated those in the
lower portion (though one major anatomical change can obviously never occur in spatial isolation from others). Almost
all nominoids share several basic features of quadrupedal
pelvic structure: in particular, elongated ischial corpora and
superoinferiorly elongated ilia whose blades lie predominantly in the coronal plane (i.e., in quadrupeds both the
ilium and the ischiopubic portion of the pelvis are drawn
out craniocaudallythe former for long excursions of the
anterior gluteals and the latter for a long hamstring moment armboth mechanically advantageous in quadrupedal
progression). They also have coronally narrow sacra and
therefore a constricted true pelvis [27]. These usually have
no serious obstetric or volumetric consequences because the
sacral promontory lies high above (superior to) the pubic
symphysis, thus providing a more than ample birth passage
[62].
A comparison of the early hominid pelvis with this more
generalized form shows that its derivation was explicitly obtained by means of two systemic changes in spatial relations:
(1) the lower trunk (lumbar column) was elongated while
(2) the pelvis was (simultaneously?) shortened and broadened. Assuming that the primary soft tissue relationships remained largely unchanged (which is, in fact, largely the case
[63]), an isolated shortening of the upper pelvis would have
107
created a spatial crisis were not some volumetric compensation have been made.
In evolutionary hindsight this took the form of a coronal expansion of the entire pelvis. AL-288-1s marked interacetabular distance is the result of an exceptionally broad
sacrum (relatively broader, in fact, than that of any primate,
including modern humans, see Figs. 5 and 11), and coronally elongated superior and inferior pubic rami (whose spatial relations otherwise remained primitive and ape-like; see
earlier). These dimensional changes accompanied a sharp
retroflexion of the ilium, creating the greater sciatic notch
(which would later be greatly enlarged by anteroposterior
expansion of the human birth canal), an abrupt superoinferior shortening of the ilium, and an internal rotation of
its anterior superior iliac spines (ASISs) from their coronal
plane (as in apes) into a more sagittal one in A. afarensis.
These changes, with lumbar lordosis, placed the anterior
gluteals in a position for effective abduction during single
support phase, but did so without any significant sacrifice of
pelvic volume or (unnecessary) expansion of the birth canal
[61,64].
An exercise that both demonstrates the uniqueness of the
pelvis of AL-288-1 and provides insight into the pattern formation processes by which it must have been genetically
conscripted is to examine proportions of hominoid sacra.
Fig. 11 presents the relative breadth of the alae for humans,
African apes, and AL-288-1. Note the extreme position of
Fig. 11. Scatter plot of S1 sacral body size (square root of [anteroposterior
diameter of S1] [mediolateral diameter of S1]) and alar breadth ([sacral
breadth mediolateral diameter of S1]/2). Alar breadth is significantly
greater in humans than in apes; in fact, average human S1 size is about
equal to that of male gorillas (the 10 gorilla specimens on the right),
whose body mass can be more than three times that of humans. This is far
in excess of what is mechanically required to resist simple compressive
loading (the JRF in the S1/L3 joint of male gorillas can hardly be less
than that in human S1/L5 joints) and probably represents the combination
of the inferiorly expanding growth gradient discussed in the text plus an
enhanced resistance to lateral bending in the elongated lumbar column.
The extreme position of AL-288-1 implies that alar breadth has essentially
remained constant as centrum size increased with body mass. This in turn
probably reflects the need to differentially increase the anteroposterior
dimension of the birth canal, rather than its mediolateral one, which has
been relatively (but not absolutely) ample since the australopithecine stage.
108
AL288-1: human sacra are much broader than those of apes,

but those of Australopithecus are even more so. This fundamental shift in pattern formation has been maintained in
modern humans as the latter substantially increased in body
size, and is fundamental evidence that the cell communication fields responsible for unique pattern formation in the human pelvis were established by the late Pliocene. Their result
was a superoinferiorly shortened, platypelloid pelvis, with
anteriorly repositioned AIISs (arising from entirely novel
centers of ossification). Their relocation, when coupled with
lumbar lordosis, resulted in an anterior gluteal placement
entirely homologous to that of modern humans. However,
their greater breadth also cantilevered the iliac blades more
prominently than in H. Sapiens [65].
5.4. Changes in the hominid pelvis during the Pleistocene
are essentially adaptations to parturition and not to
locomotion
To summarize the previous discussion, the principal adaptations of the australopithecine pelvis were as follows:
1. The anterior gluteals had been carried to a novel position
by their iliac attachments to provide pelvic stabilization
during single support phase;
2. The iliums much shortened anterosuperior height allowed lordosis at the L5(6)/S1 joint and repositioning of
the center of mass anterior to the hip and knee joints;
3. The relatively large retroauricular expansion of the ilium
placed the expanded gluteus maximus in a suitable position from which to control trunk extension at heel strike.
These changes can now serve as a background from
which to view the next major pelvic transition, that between A. afarensis and modern humans. This second phase
was not primarily directed at locomotion, but rather to the
inherent difficulties associated with birthing a fetus with
a dramatically expanded brain. Indeed, all of the significant differences between AL-288-1 and the modern human
pelvis reflect this shift.
Because the fetal brain of australopithecines was probably only marginally greater than that of modern chimpanzees, the likely sequelae of parturition can be reasonably
reconstructed (Fig. 10) [61,66]. As noted above, the locomotor adaptations of the AL-288-1 pelvis had rendered its
birth canal decidedly elliptical (platypelloid). Such a shape
has potential locomotor disadvantages without any parturition benefitit increases the moment arm of body mass.
However, no locomotor deficit was present in A. afarensis,
because its mediolateral pelvic expansion also included a
simultaneous increase in femoral neck length. There was
thus no longer sufficient selection on hip kinetics (see
below) to further alter pelvic shape.
Substantial changes in pelvic structure, however, would
have been required in order to allow passage of the increasingly massive term fetal cranium: the canal had to be made
absolutely larger, more circular, and superoinferiorly shorter
(in order to facilitate asynclitism). Such anatomical changes

must have been established during pattern formation, and
may therefore be expected to have had a multiplicity of auxiliary and pleiotropic effects. Note, for example, that the
greatly increased anteroposterior length of the modern human birth canal has resulted in a relative reduction in the
length of its superior pubic rami, as well as a shortening
of the abductor lever arm; that is, the ilium has been made
more vertical and the femoral neck shorter. These changes
resulted in a larger proportion of the entire pelvis being
devoted to the birth canal [61,66,67]. Thus, two pelvic
changes that led to a more ample pelvic inlet (and outlet) of
modern humans were: (1) a relative anteroposterior increase
in its sagittal dimension and (2) an absolute increase in its
coronal dimension. As just noted, an elevation of the anterior portion of the midplane would assist the effects of asynclitism during birthing (Fig. 10). Such a change was brought
about by a rotation of the pubic corpus superiorly (clockwise in Fig. 9) and a slight reverse rotation in the ischial
corpus (counterclockwise in Fig. 9). These changes resulted
in a more horizontal long axis in the obturator foramen and
a reduced inferior deflection of both the pubis and ischium
(which in turn reduced the separation of the ischial tuberosities from the acetabulae). Together these changes enlarge
both the midplane and pelvic outlet. Thus, the primary differences between the pelves of australopithecines and modern humans do not reflect changes in locomotor adaptation,
but instead are a complex and elaborate anatomical response
to birthing in response to increasing Pleistocene hominid
cerebralization.
5.5. The human pubic symphysis is also uniquely
specialized for parturition
There is additional telling evidence that modifications of
the birth canal played a dominant and controlling role in
guiding changes in lower limb morphology during the Pleistocene. This too, can be examined via comparative anatomy
and the fossil record.
The pubic symphysis of mammals is a site of continuous
growth in subadults. In all higher primates, including the
African apes, secondary centers of ossification for each pubic bone appear at midline and fuse to their respective pubic
corpora along with the other common osseous events of the
pelvis that occur at the end of the adolescent growth period
(e.g., apophyses for the iliac crest, ischial tuberosity, etc.).
Modern humans, however, exhibit a unique, highly delayed
pubic metamorphosis [6871]. Secondary centers of ossification do not develop until, on average, the end of the third
decade (and often do so only sporadically). This postponement of maturity has two primary effects: (1) it permits the
pubic rami to continue to expand in length even though osseous growth has ceased throughout the remainder of the
skeleton [72], and (2) it prevents premature fusion of the
symphysis before the end of the childbearing period as can
occur in other hominoids [73].
As expected, this specialized adaptation is absent in A.

afarensis. An examination of AL-288-1 shows that while
her mandible bears only a recently erupted third molar, her
pubic symphyseal face was completely mature, having the
morphology of a middle-aged human female (i.e., one
in excess of circa 35 years). This specialized delay in human pubic maturation punctuates the intense selection that
must have been operating on the adequacy of the birth canal
throughout the Pleistocene [70,74].
5.6. The kinetics of australopithecine hip joints were
similar to those of modern humans
Some years ago, before the modern principles of pattern
formation were established and both gradualism and particularism still dominated morphological interpretation, a consistent claim about the australopithecine hip was that it was
somehow incompletely adapted to bipedality because its
femoral head was perceived as being small [5]. Such an assumption was readily demonstrated to be incorrect by simple
calculations using the only complete pelvis and associated
femur available at that time, those of STS-14 [65,67,75].
The point of this examination was largely heuristicthat is,
ordinary free body diagrams of australopithecine and human
hip joints could be used to investigate the effects of slightly
different hip geometries in the two species. The australopithecines had wider interacetabular distances, but also had
longer femoral necks and greater iliac flarehip joint loading was thus about the same in both.
Recently, however, using an unusually particularistic approach, Ruff concluded that the gait pattern of AL-288-1
must have differed from that of H. sapiens [76]. His argument was as follows. He first calculated stance phase
hip joint reaction force (in units of body weight) from a
photograph of the AL-288-1 pelvis (not based on study of
the three-dimensional specimen). He obtained similar data
from McLeish and Charnleys single human X-ray [77].
Their calculations relied on known body masshis on estimated body mass. He then compared AL-288-1s femoral
109
head diameter, external proximal femoral dimensions, and

iliac thickness to those predicted for her body size from
regressions derived from other modern humans. In all of
these measurements, AL-288-1 fell well within the human
regression predictions. He then, however, concluded (quite
inexplicably) that because his single comparisons of one
australopithecine and one human indicated a higher JRF
in the former, Lucy would have been required to generate
greatly increased gluteal abductor force, ([76], p. 463),
and that her gait pattern was therefore somehow deficient
because she was not significantly more robust than modern
humans in these various characters.
The specifics are as follows. Ruff calculated a JRF of 2.17
times body weight (BW) from the McLeish and Charnley
X-ray and a value of 2.43 times estimated BW for AL-288-1
(27.4 4.4 kg). Suppose he erred slightly in the latter? Simple algebra shows that reducing AL-288-1s BW by less than
3 kg (i.e., well within the stated probable error) results in a
hip JRF identical to that of the McLeish and Charnley specimen. Put another way, do modern humans visibly alter their
gait pattern when they exceed ideal weight by 10%? Do the
increased loads that result from being slightly overweight
have any skeletally detectable effect with any reliability?
It is of particular note that Ruffs JRF value for AL-288-1
is almost identical to one we obtained for STS-14 some years
ago (2.46 BW) [67]. However that study also included 20
values for humans, and these showed a large range of JRFs
(2.262.96), differing significantly by sex. Applying identical (three-dimensional) methods to AL-288-1 yields a best
estimate of 2.28 BW. While this does not differ significantly
from Ruffs value for AL-288-1, all of our human values
were well above those obtained for the McLeish and Charnley X-ray, and AL-288-1 falls in the lower range of human
females. Furthermore, as Table 2 shows, very slight errors
in estimating the angulation of either the abductor force or
the JRF vectors cause dramatic shifts in the results. In every
anatomical character investigated by Ruff, AL-288-1 falls
directly within the range predicted by his own regressions
from modern humans, including hip joint JRF.
Table 2
Hip JRF in AL-288-1 during static single support phase
Parameter
Best estimate
Joint angle + 1
Joint angle 1
Abductor angle + 1
Abductor angle 1
JRF angle
Abductor angle
JRF
Male (N = 8), mean S.D.
Female (N = 12), mean S.D.
7.5
11.5
2.28
2.34 0.08
2.60 0.17
8.5
2.94
6.5
1.86
10.5
2.69
10.5
1.99
Data were calculated by placing the reconstructed femur and restored pelvis in anatomical position during mid-stance phase (with the medial edge of
distal femur against the midline) and estimating the line of action of the principal lateral abductors (g. medius and minimus) with a cord (as a line running
from the lateral aspect of the greater trochanter to the midpoint of the distance between the ASIS and AIIS on the iliac blade). Assuming three principal
forces (unsupported body weight, the abductors line of action, and the hip JRF), the JRF can then be calculated in units of body weight because it
must pass through the center of the hip joint in order to establish equilibrium. For greater detail of these methods, see [67]. The best estimates are
provided in column one of the table and yield a JRF of 2.28. However, note that an error of one degree in either the joint angle (i.e., the angle of the
line of action of the JRF) or the abductor angle substantially alters the resulting estimate of the JRF. Thus such calculations are primarily of heuristic
value when applied to only a single specimen. However, even with these significant errors, the resulting JRF for AL-288-1 is within the human range.
110
5.7. A further note on the sacrum of AL 288-1

The unusual breadth of the australopithecine (and descendant human) sacrum appears to have played a vital,
compound role in the development of hominid bipedality.
As we have seen, its great breadth induced a mediolateral
enlargement of the pelvis and thus maintained ample abdominal volume in the face of a precipitous reduction of
superoinferior iliac height. A progressive widening of the
australopithecine lumbar facets may have been a conjoint
result of a novel caudad-progressive increase in anlagen
(somite?) breadth culminating in the dramatic increase in
the breadth of those of S1. There would therefore seem to
be a possibility that a (the) primary adaptation to bipedality
was an increase in the pattern formation gradient yielding
increasing lumbar size caudally, along with a caudal shift
in the expression boundary of one or more Hox genes.
The great increased breadth of the australopithecine alae
functionally disengaged its PSISs and sacrum, thus simultaneously freeing the lowest lumbar vertebra from iliac
capture. An increase in sacral breadth was therefore likely
a primary one in the emergence of bipedality, and is consequently among the most diagnostic in judging the degree
of bipedal adaptation present in ancient hominids.
5.8. Particularism, adaptationism, and the interpretation
of the pelvis of AL-288-1
We will conclude this segment by briefly noting several
other claims made in the past about the pelvis of A. afarensis.
Such incidental observations have now become almost
legion and it would take an essay of prohibitive length to
discuss all of them thoroughly. We can mention only a few
typical of such claimed functional explications. Among
these are: (1) that the lunate surface of the acetabulum in

AL-288-1 lacks the large contribution from the pubic bone
that characterizes modern humans ([76], p. 287); (2) that
its AIISs are not of a form typical for modern humans,
and (3) that the hamstring surface of the ischial tuber of A.
afarensis is somehow extraordinary.
First, the ossification of the acetabulum is complex (it is
an area of principal growth in the emergence of the os coxa)
and much of the portion claimed to be supplied by the pubis
is actually supplied by the os cotyloideum. Second, the acetabulum, including its lunate surface, is highly conserved
in higher primates (not even its depth varies significantly
[78]), and it is most unlikely that any species would exhibit a
deficient acetabulum. Third, the authors making the claim
misinterpreted its structure on a cast since they misidentify
its anterior horn in their drawings. This can be confirmed
because they created an acetabular arc ratio and reported a
value of 0.78 for AL-288-1. When measured on the original
according to their definitions this index is actually 0.89 (well
within the human range). Fourth, AL-288-1 is, in fact, quite
typical of modern humans and a sizeable proportion of the
latter actually have diminutive anterior horns that are less
extensive (Fig. 12) than those of AL-288-1. The AIIS of humans is a variable osteological landmark, and there is nothing atypical whatsoever about its expression in AL-288-1.
As noted earlier, it is of a size and form characteristic of
one that has emerged by an independent apophysis (a feature shared only by australopithecines and humans), which
is, of course, the salient point.
Susman and Sterns claim in regard to the structure of
the ischial tuber is simply mystifying. As noted earlier, the
tubers structure differs substantially in humans and pongids.
In pongids the tuberosity is a single, slightly curved plane
without surface differentiation of facets for attachment of the
Fig. 12. Acetabulae of AL-288-1 (A) and of two modern humans (B and C). Contrary to claims in the literature, the surface in the australopithecine
is not deficient, but is, in fact, a typical expression of a highly variable structurethe anterior horn of the lunate surface. Note that in specimen B the
subchondral bone of the anterior horn is entirely deficient and does not extend inferiorly beyond the white arrow. Such variations in detailed anatomical
structure occur throughout the skeleton. Their use in the interpretation of individual fossils represents the error of particularism, i.e., assuming that a
single specimen represents the archetype of a species, rather than an exemplar of expression within a potential range (for discussion, see text). In fact,
all skeletons may be expected to show deviations from mean anatomical expressiononly those that lie outside the normal range of variation are of
significance in the interpretation of fossils. Note the shape and form of the AIIS in the human specimens.
three hamstrings. In humans, the tuber is distinctly faceted

and these facets are isolated from the more inferior attachment of the adductor magnus by a distinct transverse ridge
[79] (a likely insignificant pleiotropic effect of pelvic shortening). AL-288-1 is wholly like the human, and unlike the
ape in any way.
6. Summary
The adoption of upright walking occurred relatively early
in human evolutionary history. By 3 MYA, the pelvis had
been transformed from one adapted primarily to arboreal
quadrupedality as seen in living apes, to one tailored to terrestrial bipedality as seen in modern humans, including a
fully functional abductor mechanism with hip joint kinetics broadly similar our own. One of the earliest adjustments
to habitual bipedality in our ancestors was an elongation of
the lumbar spine that had been previously shortened as an
adaptation to arboreality. The unique human character of
lumbar lordosis that accompanied this elongation permitted
habitual repositioning of the HAT over fully extended lower
limbs. During the past 3 million years, primary changes in
the human spine and pelvis have centered around lumbar
re-shortening (possibly in response to selection against
scoliosis as well as flexion injury) and a restructuring of the
human pelvis so as to permit passage of large-brained term
fetuses. Much of the latter changes have centered around the
pelvic midplane and outlet. There is substantial evidence that
the muscular investments of the human thigh were demonstrably altered to accompany these changes. These will be
discussed in the next segment of this series.
Acknowledgements
I thank M.A. McCollum, P.L. Reno, B.A. Rosenman, and
M.A. Serrat for extensive critical readings of the manuscript.
Illustrations are by L.B. Spurlock and M.A. McCollum. I
thank the Cleveland Museum of Natural History for general
access to comparative specimans.
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Gait and Posture 21 (2005) 95112

The natural history of human gait and posture

E-mail address: olovejoy@aol.com (C.O. Lovejoy)

anatomy and performance. Complete answers to these kinds

C.O. Lovejoy / Gait and Posture 21 (2005) 95112

exemplars rather than as archetypes presumed to lie at

fluctuating degree states (particularism) as it is to avoid

For further discussion, see [11,12,15].

C.O. Lovejoy / Gait and Posture 21 (2005) 95112

demographically successful and capable of invading new

(from the Afar language: root [ramidus] of the ground apes

C.O. Lovejoy / Gait and Posture 21 (2005) 95112

C.O. Lovejoy / Gait and Posture 21 (2005) 95112

in the examination of the human locomotor record, but they

more extensively for suspensory locomotion than in other

C.O. Lovejoy / Gait and Posture 21 (2005) 95112

It has been argued that this widening permits greater

tally oriented. The novel orientation in humans may resist

C.O. Lovejoy / Gait and Posture 21 (2005) 95112

lordotic flexibility of the lumbar column. As with modern

the iliac crest and strong development and dorsal reflection

C.O. Lovejoy / Gait and Posture 21 (2005) 95112

Haeusler et al. recently presented detailed arguments [40]

posterolaterally repositioned shoulder girdle than occurs in

C.O. Lovejoy / Gait and Posture 21 (2005) 95112

its length, evinces clear overall short-backed morphology

C.O. Lovejoy / Gait and Posture 21 (2005) 95112

Furthermore, the argument that it is caused primarily by

Fig. 8. Superior view of iliac crest of the left innominate of AL-288-1

locomotor-related aspects of the human pelvis are present,

C.O. Lovejoy / Gait and Posture 21 (2005) 95112

which are both sagittally short (though they are markedly

noted earlier, this change in shape has almost certainly been

C.O. Lovejoy / Gait and Posture 21 (2005) 95112

single support phasei.e., one from which they could

C.O. Lovejoy / Gait and Posture 21 (2005) 95112

C.O. Lovejoy / Gait and Posture 21 (2005) 95112

AL288-1: human sacra are much broader than those of apes,

(in order to facilitate asynclitism). Such anatomical changes

C.O. Lovejoy / Gait and Posture 21 (2005) 95112

As expected, this specialized adaptation is absent in A.

head diameter, external proximal femoral dimensions, and

C.O. Lovejoy / Gait and Posture 21 (2005) 95112

5.7. A further note on the sacrum of AL 288-1

these are: (1) that the lunate surface of the acetabulum in

C.O. Lovejoy / Gait and Posture 21 (2005) 95112

three hamstrings. In humans, the tuber is distinctly faceted

C.O. Lovejoy / Gait and Posture 21 (2005) 95112

[56] Stern JT, Susman RL. The locomotor anatomy of Australopithecus

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