¿ìè¶ÌÊÓƵ

Ever since Plato described humans as ‘featherless bipeds’, we have recognised
walking upright on two legs as a defining characteristic of humankind. The
fossil record shows that bipedalism is very ancient, predating tool-making
and the evolution of large brains that were once seen as the most fundamental
biological adaptations of humankind. Yet precisely when bipedalism evolved
– and what part it played in how our ancestors moved about – remains disturbingly
elusive. New clues to the timing of bipedalism, though, are being gleaned
from a surprising source: the bony structure of the inner ear. If the research
is right, our ideas about how bipedalism developed – and even the identity
of our ancestors – will need a radical rethink.

The ear would seem to have little to do with pinning down the origins
of bipedalism. A more obvious approach is to analyse leg bones from various
fossil hominids for signs of the biomechanical and structural adaptations
that made it possible to take the weight on the hind legs and to balance
on one leg as each stride is taken. Indeed, many such adaptations are seen
in Australopithecus afarensis, the earliest known member of the human lineage,
who lived between about 2.5 and 4 million years ago. Unfortunately, leg
bones cannot tell the entire story, and evidence from the arm bones tells
a different story.

Analysis of the arm bones reveals that A. afarensis had long muscular
arms, mobile shoulders and ape-like elbows. To some palaeoanthropologists,
this suggests that A. afarensis had a chimp-like predilection for agile
climbing in trees combined with more human-like bipedal movements on the
ground – a locomotor repertoire practised by no living primate. To others,
the leg and arm bones indicate that A. afarensis walked around upright and
that the hefty arms are simply hereditary leftovers from a more ape-like
ancestor.

But there are serious disputes over the significance of anatomical features
like these when it comes to reconstructing ancient modes of moving. At
the crux of the controversy are fundamental and thorny issues. Do behaviour
and anatomy always go hand in hand? How should we weigh the relative importance
of habitus (behaviour during life) and heritage (evolutionary ancestry)?
This boils down to tough questions over specific specimens, such as the
heavily muscular humerus bones of A. afarensis found during the past four
years at Maka and Hada in Ethiopia. Does the extreme robustness of these
arm bones reflect the demands of habitual tree-climbing – or are they evidence
of powerful forelimbs, still useful to A. afarensis but largely bespeaking
the arboreal heritage of its forebears? There is no consensus.

There is another, more subtle issue. Bipedalism has long seemed a solely
human attribute, one of the last survivors of a list that once included
tool-making, large brains and language. Assigning full bipedalism to a
fossil hominid carries with it an aura of humanity that seems incongruous
to those who see early hominids as essentially ape-like. Conversely, those
who detect the origins of many human behaviours among our earliest ancestors
are eager to see australopithecines or early Homo as fully bipedal.

Into this maze of opinion and interpretation has come an entirely new
perspective on the way anatomists reconstruct the modes of moving practised
by extinct species. Fred Spoor, a Dutch anatomist who has recently moved
from the University of Liverpool to University College London, has begun
to explore a previously untapped source of information about locomotion
and posture – the bony labyrinth of the inner ear.

Steadying influence

In all mammals, the bony labyrinth is a tiny, intricate structure in
the skull that houses important sensory organs. The most obvious is the
organ of hearing, part of which is found in the cochlea, a coiled section
of the labyrinth that resembles a snail’s shell. But of special importance
is the vestibular system, which functions as the organ of balance or equilibrium,
and is also partly located in the bony labyrinth.

Spoor focused on the part of the vestibular system known as the semicircular
canals – three bony tubes that curve through the bone that underlies the
external ear. The anterior, posterior and lateral semicircular canals are
arranged at roughly right angles to each other and are lined, in life,
with a fluid-filled membrane. Cells in the membrane sense displacements
of the head and body, sending messages to the muscles of the eye that generate
an ocular reflex which enables the eyes to maintain a steady image of the
world even when the head (or body) is moving.

To understand this reflex, try a simple exercise. Hold your head still
and wiggle your copy of ¿ìè¶ÌÊÓƵ rapidly. You will find it is impossible
to keep reading when the object of your vision moves, because your eyes
cannot adjust rapidly enough to the changing position of the paper. Now
hold the magazine still and wiggle your head rapidly: you can keep reading
because the semicircular canals tell your eyes how to move relative to
your head in order to maintain a stable image of the world. Although reading
while moving may be of little evolutionary importance to our ancestors,
being able to see clearly and accurately what they were walking on or
clinging to may have been vital, whether they ran along the ground or swung
through the trees.

Monitoring movement

As well as maintaining this ocular reflex, the semicircular canals also
send messages to the muscles that control the position of the head and the
posture of the body so that movement is smoothly regulated. The sensitivity
of the vestibular system is tuned in different organisms by variations in
the dimensions of the semicircular canals, particularly the radius of curvature.

The functional role of the vestibular system led Spoor to think that
the structure of this part of the skull might reveal important and novel
clues about the origins of bipedalism. Some previous studies had shown a
relationship between the size or shape of the bony labyrinth and modes of
movements in birds and a few species of primates, in that faster-moving
animals tend to have bigger semicircular canals. Spoor realised that just
as balancing on two legs instead of four requires a massive reorganisation
of the leg, so too, it would require a dramatic reshaping of the semicircular
canals. All he had to do was find a way to visualise the shape and dimensions
of these tiny structures – the labyrinth is generally about 1 centimetre
across at most – buried deep within the skull.

Traditional methods were unsuitable for large-scale, comparative studies
involving rare hominid fossils or skulls of primates under threat. It was
impossible to use methods such as serial sectioning – slicing a skull up
like a loaf of bread – or injecting latex into the inner ear and dissolving
away the surrounding bone. So with help from Frans Zonneveld, an imaging
expert at Utrecht University Hospital in The Netherlands, Spoor turned
to high-resolution computerised tomography, or CT scanning, a biomedical
technique in which objects are ‘serially sectioned’ radiographically. By
building up a series of images of radiographic slices through a fossil or
skull, Spoor could make an accurate three-dimensional reconstruction of
the bony labyrinth of skulls ranging in size from small squirrel monkeys
to hulking gorillas.

Spoor decided that he needed a large, comparative database to provide
the framework for interpreting data on controversial early hominid specimens.
He scanned almost a hundred specimens of extant or recently extinct primates
of known locomotor habits, including prosimians such as pottos and lemurs,
a variety of monkeys, apes ranging from gibbons to gorillas and chimps,
and modern humans. He also scoured the scientific literature for scans of
another 70-odd extant primates.

The scans showed without a doubt that the size of the bony labyrinth
reflects patterns of movement. Fast-moving, agile primates such as the
gibbon, which swing through trees, have canals with a larger radius of curvature
than more ponderous species such as the gorilla. The database also showed
that the critical factor was rapidity of movement and not whether movement
occurred in trees or on the ground. When Spoor calculated the size of the
labyrinth relative to body size, small slow-climbing pottos, who spend
most of their time in the trees, fell into the same group as large, slow-moving
quadrupedal gorillas who generally move on the ground.

The configuration of semicircular canals in humans stood out as the
most distinctive of all the species Spoor studied. The precarious task
of pivoting around one leg while the other leg swings forward to take a
new step has shaped the human bony labyrinth in unique ways. Compared to
great apes (whose locomotor repertoire is probably close to that of the
last common ancestor of apes and humans), we have larger anterior and posterior
semicircular canals and a smaller lateral canal. This arrangement is geared
toward monitoring movements that occur in a vertical plane – as is the
case in bipedal walking or running.

Scanning skulls

The task of compiling this comparative sample alone was impressive,
but Spoor moved on to study a series of 20 fossil specimens from early
to late hominids. Unfortunately, he has not yet been able to arrange to
scan an A. afarensis skull, but he has examined two subsequent species
in that genus, A. africanus and A. robustus (sometimes known as Paranthropus
robustus). He also scanned two species of Homo that many see as descendants
of A. africanus: H. habilis, the earliest member of our own genus, and H.
erectus, the species that precedes modern humans. H. erectus is not only
larger-bodied and bigger-brained than all previous species but shows many
anatomical adaptations to full bipedality. H. habilis, however, is a perplexing
species, because the size of body and brain in some individuals is much
smaller than in others.

The smaller type is represented by specimens such as the partial skeleton
from Tanzania known as Olduvai Hominid (OH) 62, which includes fragments
of skull, teeth and limb bones. Although H. habilis would be expected to
be more human-like than its australopithecine ancestors, Sigrid Hartwig-Scherer
and Robert Martin of the Anthropological Institute of Zurich University
found the opposite when they analysed the limbs of OH 62 in 1991: the limbs
have more primitive or ape-like features than does Lucy, the partial skeleton
of A. afarensis.

Furry grandfathers

In contrast, some of the limb bones found and attributed to H. habilis
are larger and more modern-looking, while there are skulls – such as the
specimen from Koobi Fora, Kenya, known by its museum number KNM-ER 1470
– with brains much larger than that of specimens like OH 62.

The striking differences between the large and small individuals has
led Hartwig-Scherer, Martin and others to suggest that two different species
are being grouped into H. habilis, and only one is part of the modern human
lineage.

Thus the anthropological community watched Spoor’s research with keen
interest, waiting to see what it might reveal about the apishness (or humanness)
of our early ancestors. Were australopithecines furry humans – or were
they simply upright apes? Was H. habilis a taxonomic muddle of several species
– or was it our long-armed great-great-grandfather?

The scans of the australo-pithecines told a consistent story: the bony
labyrinths in all individuals of both species were decidedly ape-like.
In contrast, the proportions of the semicircular canals in H. erectus skulls
were similar to those found in modern humans. Spoor sees this as evidence
supporting the theory that australopithecines mixed climbing in trees with
terrestrial bipedalism. In a paper published in Nature on 23 June with Zonneveld
and Bernard Wood of the University of Liverpool, Spoor suggests that australopithecines
were probably not obligatory bipeds, but facultative ones – meaning that
they could move on two legs competently enough but were not so thoroughly
adapted to bipedalism that anything else was awkward.

Spoor’s team also speculates that australopithecines might have balanced
on two legs when standing rather than when moving, echoing a hypothesis
put forward earlier this year by Kevin Hunt of Indiana University. Hunt
had been studying chimps in Tanzania, and observed that they stand on two
legs mostly when they are gathering fruit from small trees in open forests
and woodlands; they often grasp an overhanging branch with one arm to steady
themselves while they stand and feed. If they move a short distance to another
patch of food, the chimps may stay upright – a pattern Hunt feels is a useful
model for the evolution of hominid bipedalism. Perhaps our ancestors, too,
first adopted bipedalism as a feeding posture and only later evolved the
complex adaptations of back, hip, leg and balance that form the basis of
our unique way of moving.

Enigmatic labyrinths

Glenn Conroy of Washington University School of Medicine in St Louis
is enthusiastic about Spoor’s work. In collaboration with Michael Vannier
of the same institution, Conroy pioneered the application of CT scanning
to fossil hominids. Says Conroy, ‘I think what Fred’s work is doing is using
a totally independent anatomical system to reinforce the growing evidence
that australopithecines’ postcrania (the limb bones) aren’t fully modern
in terms of locomotion.’

But the most enigmatic result was that from the scan of H. habilis.
Unfortunately, Spoor was able to scan only one skull, that of StW 53 from
Sterkfontein, South Africa, which is the small type. Its labyrinth had a
particularly large lateral semi-circular canal, making it unlike those of
the other fossil or modern hominids as well as being distinctly different
from those of the living great apes. ‘It’s very difficult to interpret,’
says Spoor. ‘The only thing that the labyrinth suggests is that (H. habilis)
is less bipedally adapted than the australopithecines. It looks much more
like gibbons, maybe, or like baboons – certainly not a human pattern.’
His conclusions is that: ‘Either this specimen is not H. habilis, or if
it is, H. habilis is unlikely to be ancestral to H. erectus,’ which – not
surprisingly – has entirely human-like labyrinths.

Martin welcomes Spoor’s finding, which confirms the conclusion that
he and Hartwig-Scherer reached in their analysis of the limbs of the smaller
type of H. habilis. On the basis of the two independent studies, Martin
is prepared to endorse a radical conclusion: ‘The combined evidence now
suggests that we in fact have before us the remains of a distinctive hominoid
from Africa, but of a great ape rather than a hominid.’

Not all palaeoanthropologists are prepared to endorse his conclusions
wholeheartedly at this stage. For example, Henry McHenry of the University
of California at Davis feels more evidence is needed to answer the question:
how different can two labyrinths be and still reflect the habitual patterns
of movement of a single species? Indeed, McHenry and others question how
directly labyrinth size and shape reflects locomotion at all. ‘Per-haps
the inner ear is showing something quite different from posture,’ McHenry
says, ‘but I can’t wait until he does 1470 from East Africa.’ If the larger-bodied
specimens have more human-like labyrinths than StW 53, this will provide
additional evidence that H. habilis is a muddle of two different organisms.

Steve Ward, an anatomist at the Northeastern Ohio University College
of Medicine, is also wary of revising theories on the basis of Spoor’s preliminary
results, but says, ‘Every once in a while someone comes along and unlocks
a new door that makes it possible to look at things that have been lying
around unanalysed. Whatever the ultimate outcome of this work, it is a pioneering
approach. Even if you disagree with the conclusions, this work is important.

Pat Shipman is an anthropologist and freelance writer living in Maryland.