Naturalis Historia: Volume IV

(originally written for my Evolutionary Theory class)

Evolution of Bipedalism in Hominids

“We must, however, acknowledge, as it seems to me, that man with all his noble qualities… still bears in his bodily frame the indelible stamp of his lowly origin.”
– Charles Darwin, The Descent of Man (1871)

Humans are unique in the animal kingdom as being the only habitual terrestrial biped built for upright walking. Homo sapiens were not alone, however; a diversity of bipedal hominids thrived before us. Being adapted to bipedal movement changed the morphological structure and even behavior of these early hominids, but why did certain species make the transition to bipedal movement? There are many theories as to the origins of bipedalism and the reasons that led these hominids to walk upright. From examining the fossil record and modern primate behavior and anatomy, insights on the evolution of bipedalism can be uncovered.

In the 18th century, noted taxonomist and naturalist Carolus Linnaeus recognized the relationship between humans and apes. In his Systema Naturae, published in 1736, he was the first to place humans together with other primates in a group he named Anthropomorpha (Lewin 1999:2). He considered that the great apes were the closest living relatives of humans based on morphological similarity. The idea of the biological evolution of the human species was not legitimized until Darwin published On the Origin of Species in 1859, even though he did not specifically address human evolution. In 1864, Darwin’s friend Thomas Henry Huxley published a book entitled Evidence as to Man’s Place in Nature. The book was based on evidence from comparative anatomy among apes and humans in which he concluded that humans shared a close evolutionary relationship with the great apes (Lewin 1999:2). By this time, scientists were aware of past human ancestors due to the discovery of Neanderthal bones in Germany in 1856. However, it was not until 1924 when the first hominid fossils were found in Africa. The Taung skull, discovered in a cave deposit in South Africa, was the first fossil to provide evidence for bipedal movement in hominids. The anthropologist and anatomist Raymond Dart described the skull as being a unique species of early human, Australopithecus africanus. The remains consisted of a small skull with the position of the foramen magnum at the base of the skull indicating bipedal movement.

The Earliest Known Hominoids
Australopithecus africanus lived around 3.9 millions years ago and was considered to be fully bipedal. The evolution of bipedalism began much earlier, however, with the early Miocene apes who where creatures of the tropical and subtropical forests. Around 22 million years ago, the split between the lesser apes and great apes (including humans) is thought to have occurred. The supposed last common ancestor before this split is the Miocene ape Proconsul africanus (Lewin 1999:89). This ape was an arboreal quadruped that had a mixture of both ape and monkey characteristics, including opposable thumbs (suggesting manipulative skills) but no tail. It moved on all four legs and its thorax was narrow and deep, a characteristic seen in pronograde (body horizontal to the ground) monkeylike locomotion, while the shoulder and elbow regions were apelike (90). By 13 millions years ago, Miocene apes were still quadrupedal and living in trees. Pierolapithecus, discovered in 2002, could possibly be the last common ancestor of humans and great apes. The partial skeleton displayed an orthograde posture (upright posture with the body more vertical to the ground) as an adaptation to vertical climbing and suspending the body from vertical branches (Moyà-Solà et al. 2004). The Dryopithecus species, an ape that lived around 9.5 million years ago, had long arms and short legs and appeared similar to modern day orangutans, which hang from branches and move slowly through them (Arsuaga & Martinez 1998:33). The postcranial anatomy of Dryopithecus reflects a more orthograde posture than seen in other Miocene apes because, for example, the lumbar vertebrae are shorter, the arms are more powerful and the hands are larger (Lewin 1999:91).

The chimpanzee-human split is believed to have occurred approximately 7 millions years ago with the last common ancestor being Sahelanthropus tchadensis, an ape with an anteriorly placed foramen magnum that may suggest bipedalism, although it is still debated (Brunet et al. 2002). After this split, the branch that led to modern day chimpanzees became more specialized in climbing trees with a bent knee posture while human ancestors began to develop bipedal movement. One of the earliest human ancestors after this split was Orrorin tugenensis, a hominid that lived 6 million years ago. It was discovered in 2000 in Kenya and its find is significant because it represents the earliest hominid species with evidence of bipedal movement (Pickford & Senut 2001). These findings now suggest that bipedalism may have arisen during the chimpanzee-human split, which is much earlier than previously assumed.

The Orrorin fossils found consisted of a femur that suggests it walked upright, a humerus shaft suggesting tree-climbing but not brachiation (a form of arboreal locomotion that involves swinging from branch to branch using only the arms), and the presence of the obturator externus groove on the femur that indicates bipedal movement since the obturator externus muscle is important in bipedal locomotion and originates in the pubis region of the pelvis and inserts into the trochanteric fossa of the femur. The Orrorin findings support the theory that the origins of bipedalism occurred in an arboreal precursor living in a forest and not a quadrupedal ancestor living in open country. It was traditionally assumed that bipedalism arose 4 million years ago in the Pliocene with Ardipithecus and Australopithecus; however, the recent finds of Orrorin seem to disagree with that view. The hominid Ardipithecus ramidus lived around 4.4 million years ago in a forested habitat and habitually walked upright, from evidence of its foramen magnum, femur fragments, and its toe structure. It appears A. ramidus was a forest-dweller because many of the types of mammals with which the hominid was found were also forest-dwellers (colobus monkeys and antelopes). Also, the outer layer of enamel on the teeth is thin and similar to chimpanzees, which eat fruit, leaves, shoots, and other plant products, so the conclusion has been that the first hominids lived in forests (Arsuaga & Martinez 1998:51-53). Since A. ramidus lived in the forests rather than open grasslands, it poses problems with some theories that suggest bipedalism arose in the savannah.

The australopithecines were hominids that lived in Africa between 2-4 million years ago and are thought to be fully terrestrial bipeds. Fossil evidence from australopithecines also supports the view that bipedalism predated large brains since australopithecines had small brains. Even though australopithecines were bipedal, they still exhibited adaptations to tree climbing, and some researchers support the view that they were partially arboreal and may not have had a full striding gait, but more of a bent-knee posture similar to chimpanzees (Lerwin 1999:106). The curvature in the phalanges reflects their ability to grasp and climb branches. A cranially orientated shoulder joint, shorter hind limbs, long arms, and a greater mobility in the wrist also supports the notion that australopithecines had arboreal adaptations (106). The evidence that strongly suggests bipedalism consists of the pelvis, femur, and feet. The iliac blades of the pelvis are far wider and shorter much like humans, in contrast to chimpanzees, which have longer and narrower blades. The sacrum is wide and positioned directly behind the hip joint and there is evidence of a strong attachment for the knee extensors. The femur also angles in toward the knee, which would have allowed the foot to fall closer to the midline of the body, a trait of habitual bipedal movement. The foot also features a big toe parallel with the others, making it difficult for grasping branches. It is probable their upright gait was similar to modern humans since it would have been more efficient than bent-knee walking, and the Laetoli footprints indicate an arch in the foot and no opposable big toe (Sellers et al. 2005).

Origins of Bipedalism
It is clear that many primate species had lived successfully in the trees, so why would a certain species risk changing its behavior and become bipedal? Various selective pressures have been suggested as to why early hominids made the transition to bipedalism, such as the need to carry objects and offspring, increased energy efficiency, to reduce the amount of skin exposed to the sun, predator avoidance, acquiring new food, or responses to climate changes (Lewin 1999:93). If bipedalism did occur during the chimpanzee-human split, then it is proposed that human ancestors made the transition to upright walking while chimpanzee and gorilla predecessors adapted to arboreal movement. The quadrupedal to bipedal transformation may also not be as dramatic as it may appear, since primates are not true quadrupeds in that their body posture is often upright, such as in tree-climbing, and chimpanzees and gorillas knuckle-walk and exhibit a slight upright posture, although with bent-knees (Lewin 1999:94-95). The great apes walk upright with bent knees and flexing the hips because of differences in the pelvis. In humans, we have abductor muscles that keep the pelvis vertical and balanced when we take strides. However, in chimpanzees, their muscle fibers are oriented toward the back so to keep from falling when walking upright, they must shift their trunk forward to support themselves (Arsuaga & Martinez 1998:67-68).

There are basically two general views on the origin of bipedalism in hominids: the ancestor was a terrestrial knuckle-walker or a species living in the trees that adopted a vertical posture (Lewin 1999:81). From these two perspectives, numerous hypotheses for the origins of bipedalism have been developed including the postural feeding hypotheses, the provisioning model, behavioral models, thermoregulatory model, carrying model, savannah hypothesis, aquatic ape hypothesis, and the squat-feeding hypothesis. However, a number of forces may have acted together so these hypotheses should not be considered mutually exclusive.

The postural feeding hypothesis suggested by Hunt (1996) asserts that arboreal food gathering and vertical climbing influenced anatomy. Modern chimpanzee behavior indicates chimps are bipedal when gathering food: on the ground they reach up for fruit and in trees they grab overhead branches. Movements coevolved with chimpanzee arm-hanging, as it was efficient in gathering food, and it has been discovered that A. afarensis had similar features for arm-hanging in the hand and shoulder inferring australopithecine adaptation to arboreal bipedal fruit gathering.

There are a variety of behavioral models that suggest that specific changes in behavior were the driving force for bipedalism (Lewin 1999:93), including sexual selection, escape from predators, and bipedal threat displays (Jablonski & Chaplin1993), although these tend to be circumstantial theories with no traces in the fossil record. Many support theories involving the need for carrying objects that drove the change to bipedalism since chimpanzees are known walk upright and carry tools, although only for very short distances. However, if bipedalism arose around 7 million years ago, then it predates tool-use by as much as 4 million years (Lewin 1999:96). Also, hominids at this time were primarily gathering food, not hunting, so gathering food may have contributed to bipedalism.

The provisioning model proposed by Lovejoy (1981) incorporated the carrying model with behavior, suggesting that bipedality was a response to monogamous society. Hominid males would leave their mate and search for food in order to ensure the female would have enough nutrition and bear more offspring. The only efficient way to bring back food was to be bipedal. However, there is evidence against monogamy in hominids. Sexual dimorphism is reduced in monogamous primates but in australopithecines, males were much larger than females. Also, monogamous primates are territorial but A. afarensis were thought to live in groups (Stanford 2003:113).

The savannah hypothesis is based on the climate changes that occurred in east Africa that caused openings in the forest and so a mixture of savannah and scattered woods may have forced hominids to travel between clusters of trees and bipedalism offered greater efficiency for slow, long-distance travel between these clusters (Stanford 2003:95). Hominids would have had to travel relatively long distances while carrying objects, thus making qudrupedalism extremely inefficient.

The thermoregulatory model (Wheeler 1991) suggests that since bipedalism causes increased heat loss and cooling, reduced heat gain and water requirements, it was a selective force in tropical climates. Being bipedal allows an individual to be higher above ground, with more access to winds and a vertical posture that allows less body to be directly exposed to the sun. However, some evidence disagrees with the thermoregulatory model, such as how australopithecines lived in wooded and well-watered environments and would not have directly needed protection from the sun. Bipedalism was well established before the dramatic change in African ecology and before the longer leg length as seen in Homo species. Therefore, Homo species were probably more adapted to the savannah than australopithecines; so living in the savannah was a later adaptation and not a driving force for bipedalism (Stanford 2003:96).

The aquatic ape hypothesis is a speculative theory in which Morgan (1997) claims that bipedalism arose as a result from bipedal wading and provided the advantage of keeping the head above water for breathing. According to this theory, hominids lived close to water, gathering much of their food in or near the water and adapting new modes of locomotion in order to move and gather food in the water. Morgan cites our relative hairlessness, increased subcutaneous fat and sebaceous glands as changes in anatomy. However, all of these claims can be attributed to other purposes and there has been no fossil evidence of hominids suggesting they were found in water (Stanford 1999:109). A hypothesis proposed by Kingdon claims that foraging on the ground in a squatting position demanded the necessary modifications to culminate bipedal walking, since it allowed the feet to change from being graspers to platforms in order to have a steady stance (2003:19).

Walking Upright
Primates constitute a very homogeneous set of species in terms of ecological adaptations, such as living in humid tropical forests, in mountain regions, or on the open savannah, and are varied in terms of their diet. Having evolved in the trees, modern primates, including humans, all share unique arboreal features such as the ability to grasp and climb branches, having a large big toe as opposed to the other toes, flat nails on the digits of the hands and feet instead of claws, and flexible shoulders that suggest a protobrachiator ancestor (Arsuaga & Martinez 1998:18-19). When great apes walk on the ground, they generally move on all four limbs but their trunk does not become horizontal like in other quadrupeds; instead it slopes downward and they support themselves on the backside of their phalanges (knuckle-walking). The great apes also move bipedally in trees, grasping branches with their arms and walking on their hind limbs (26).

Adaptations to bipedalism include several skeletal changes: a vertically held head, shortened forelimbs, short and wide pelvis, increased hind limb length, increased valgus angle of the knee, hands with enlarged thumbs but non-curving fingers, platform feet with non-opposable big toes in line with the other non-curved toes, a curved lower spine, extensible knee joints, and a foramen magnum moved toward the center of the basicranium (Lewin 1999:81). The valgus angle of the femur provides the femur to angle in toward the knee so the foot can be placed underneath the center of gravity while striding. The valgus angle is apparent in australopithecines while the great apes have no angle (95). The foot in hominids is designed as a walking platform to support weight rather than act as a grasping structure as in other apes. The big toe is non-opposable and the foot has an arch to transmit weight from the heel, along the outside of the foot, to the big toe. The foramen magnum (opening at base of skull through which the spinal cord enters the cranium) is located toward the center of the cranium as opposed to the back as in apes because the skull is perched atop a vertical spine in a biped (96).

A New Kind of Hominid
The advantages to bipedalism caused hominids to adapt to a new niche; it encouraged hominids to use this opportunity to acquire new food and travel long distances. In order for bipedalism to have become successful, it had to affect the daily lives of hominids, such as finding food and mating (Stanford 2003:115). Since other animal species obviously must avoid predators and also adapted to changing African environments without becoming bipedal, something important triggered and benefited these hominids into walking upright. Foraging and acquiring food is one of the most important influences on behavioral and anatomical changes (Standford 2003:128). By being the most advantageous way for certain hominids to acquire food, bipedalism acted as an evolutionary pressure on these hominids to become successful in their environment. Early hominids probably lived in a variety of habitats and bipedal walking would not have been beneficial in all settings, just in forested areas where fruits grow in abundance on the ground and in small trees, or where forest clusters are separated (137).

Walking upright caused hominids to free their arms and be able to use them as manipulative structures in gathering food. Upright walking also proves to be more energy efficient than knuckle-walking and would have been beneficial in exploiting resources that demanded a more energy-efficient mode of travel (Lewin 1999:96). Bipedalism would eventually lead to behavioral changes, such as prolonging childhood since infants had to be carried since they lost their ability to grasp on by themselves, and perhaps changes in social structure, since caring for infants limited the mother’s ability to care for herself and needed support from others.

Current research has favored the idea that bipedalism evolved as a particular way of getting food in trees (Stanford 1999:120). Since it is now known that early hominids lived in forests and not the grasslands, they did not have to adapt to changes in the environment. Bipedalism offered an advantageous and energy efficient way of acquiring fruit in trees by moving on two legs and hanging by their arms for balance, and findings based on Orrorin fossils support this idea that bipedalism arose in an arboreal setting. The short lower limbs and broad pelvis of early bipedal australopithecines are arboreal adaptations, not terrestrial, as are long forelimbs enabling greater access to food and facilitating arm-hanging. Research on orangutan behavior also supports an arboreal origin since orangutans extend their legs at the knee and hip to give them a straighter posture in order to reach fruit (Thorpe et al. 2007).

The Downside of Being Bipedal
Evolutionary trade-offs existed from the switch to bipedal movement. As it gained energy efficiency from striding, bipedalism caused hominids to lose their efficiency for climbing. The changes in the pelvis caused the birth canal to dramatically narrow and the head of the newborn must twist in order to exit the birth canal, making the mother unable to see her newborn’s face and assisted childbirth beneficial (Stanford 2003:53-56). Some features of the human skeleton are poorly adapted to bipedalism; human joints are forced to support weight for which they were not originally designed for, now that the body’s full weight is on two legs rather than four. This leads to joint problems and also back pains due to lumbar lordosis, a curve in the spine for support and stability but can result in lower back problems (56-57).

In conclusion, bipedalism has a complicated evolutionary history, mainly due to lack of fossil evidence. Many advantages to bipedalism are apparent but the ones that were most influential to hominids will be difficult to undercover. Current research favors the arboreal origin, with acquiring food as the primary motivator for bipedal movement. New findings of even older bipedal hominids (Orrorin) suggest that our understanding of bipedalism is still being questioned. Views are constantly changing and bipedalism is no longer considered to have occurred around 4 million years ago, but actually much earlier. Knuckle-walking predecessors are no longer in favor, as is attributing bipedal walking to changes in habitat. New discoveries remain to be seen where it will take the origins of bipedalism.

References Cited:
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Brunet, Michel, et al. 2002. A new hominid from the Upper Miocene of Chad, Central Africa. Nature 418:145-151.

Hunt, Kevin D. 1996. The postural feeding hypothesis: an ecological model for the evolution of bipedalism. South African Journal of Science 92:77-90.

Jablonski, N.G. and G. Chaplin 1993. Origin of habitual terrestrial bipedalism in the ancestor of the Hominidae. Journal of Human Evolution 24:259-80.

Kingdon, Jonathan 2003. Lowly Origin: Where, When, and Why Our Ancestors First Stood Up. Princeton: Princeton University Press.

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—————- 1999. Human Evolution: An Illustrated Introduction. Malden, MA: Blackwell Sciences.

Lewin, R., Swisher, C., Celso, C., and Garniss, H. 2000. Java man: how two geologists’ dramatic discoveries changed our understanding of the evolutionary path to modern humans. New York: Scribner.

Lovejoy, Owen 1981. The Origins of Man. Science 211:341-348.

Morgan, Elaine 1997. The Aquatic Ape Hypothesis. London: Souvenir Press.

Moyà-Solà, Salvador, Meike Köhler, David M. Alba, Isaac Casanovas-Vilar, and Jordi Galindo 2004. Pierolapithecus catalaunicus, a New Middle Miocene Great Ape from Spain. Science 306:1339-1344.

Pickford, M. and Senut, B. 2001. ‘Millennium ancestor’, a 6-million-year-old bipedal hominid from Kenya. South African Journal of Science 97. 1-2: 22.

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Stanford, Craig 2003. Upright: The Evolutionary Key to Becoming Human. New York: Houghton-Mifflin.

Thorpe, SKS, Holder, R and Crompton, RH. 2007. Origin of human bipedalism as an adaptation for locomotion on flexible branches. Science 316:1328-1331

Wheeler, P. E., 1991. The thermoregulatory advantages of hominid bipedalism in open equatorial environments: the contribution of increased convective heat loss and cutaneous evaporative cooling. Journal of Human Evolution 21:107-115.