Lowly origin of bipedalism :: the squatting model

In his 2003 book, Lowly Origin, Jonathan Kingdon presents a model for the origins of hominid bipedality, along with many other possible insights concerning the evolution of both earlier apes and later hominids. The book is notable because of Kingdon's speciality: as a very talented zoologist and perhaps the foremost biogeographer of African mammals, he brings an eye toward the temporal and spatial context of the transition to bipedalism that is generally lacking in other models. The book is also notable because it is recent, and provides a present-day look at many venerable models of hominid origins that well characterizes their strengths and weaknesses with respect to the present pattern of evidence.

An example of his biogeographical knowledge coming into play is his hypothesis for the place that bipedalism may have originated. Many models talk about a hypothetical division between Central African and East African forests or a hypothetical mosaic forest-savanna woodland mix. Kingdon can talk about actual forests where this might have happened. He focuses on the coastal African forest, which stretches from Somalia to South Africa (116-119). His examinations of biogeography of microfauna have shown that this forest has been biologically separate from those of Central Africa for a very long time. Today, the coastal forest is depauperate of large and medium-sized endemic mammals, which Kingdon attributes to human activity during the past 40,000 years. In the past, this forest would have served as a core area for animals spreading periodically into river valleys and forest fragments further inland. It would also have presented a rather different climate regime from the West and Central African forests, with its highly seasonal monsoonal rainfall.

Filling the bill

Any model that attempts to explain hominid origins must provide an account of several distinct things:

  1. How did early hominid populations become separated from early chimpanzee populations? That is to say, what accounts for the human-chimp divergence?
  2. What decisive advantage was there in increasing the frequency or importance of bipedal locomotion?
  3. What exactly was the ancestral pattern of locomotion?
  4. Why did this ancestral pattern, whatever it was, lose its advantages when compared to bipedality?

To question number 1, Kingdon gives basically the same biogeographical answer as Coppens' East Side Story and many others: namely, that progressive aridification of East Africa led to a separation of East and West African ancestral hominoids. His details about the nature of the East African forest are very welcome and interesting, but do not change the basic picture. Kingdon places the timing of this event in several cycles of aridity beginning at 10.5 million years ago, through recurrent drying at around 7.8 million years ago and 6.2 million years ago (119). These dates do approximately correspond with the time interval preceding the fossil remains of the earliest hominids, which are now some 6 million years old.

To the second question, about the advantage of bipedalism, Kingdon provides an answer based on Clifford Jolly's (1970) seed eaters hypothesis. In this model, and upright posture for the upper body is advantageous for use in foraging for small items, in particular seeds from grasses. Like Jolly, Kingdon envisions a squatting, ground-based ape, which he calls the ground ape. He describes the effects of a small item feeding strategy as follows:

One way of asking how apes might have responded to these limitations is to look at the feeding strategies of living species. For example, when contemporary chimps are under duress from a poor fruit season, they break up into smaller foraging units that scour the environment more thoroughly while trying to maintain their frugivorous dietary preferences for as long as possible. By contrast, the more terrestrial gorillas respond to the same pressure by maintaining their groupings but diversifying and enlarging the range of their foods to include previously ignored and less digestible plants. Another variant, better suited to eastern forests, would have been to diversify (by including more animal and underground foods) but also to spend more time and effort foraging for smaller (but still nutritionally rewarding) items. As observed in contemporary situations, these are stopgap routines for gorillas and chimpanzees. However, I am proposing that similar strategies could develop or be transposed into a sustained and systematic way of using a spatially restricted environment. (122-123)


When Jolly originated the small object feeding model, he focused on the analogy between geladas and savanna baboons as a way of understanding the effects of this dietary change. Kingdon focuses more closely on the range of plant species that may be exploited by such a dietary shift, the ability of ancient groups to exploit the same geographic range more intensively, and the probable ecological diversity of plant species in the East African forest. He notes that chimpanzee groups across Africa appear to use a similar number of fruiting plant species, adjusting their home range in response to habitat richness. This results in a great disparity in chimpanzee foraging ranges (from as little as five square kilometers to as much as 400 square kilometers). Kingdon suggests that a more intensive foraging strategy based on the wider ecological diversity of East African forests may have increased the carrying capacity of these forests for the ground apes, with consequent alterations in their social behavior and ecology. He supports this ecological model with an analysis of the species richness of human-edible plants in this eastern forest (123). His major case is based on the increased availability of ground or near-ground foods in the eastern forest, including both animal and plant resources, compared with the small ratio of time that forced chimpanzees appeared to spend foraging near the ground as opposed to foraging canopy fruits

Perhaps the most important change, in answer to question 4 above, is a change in daily foraging range. As Kingdon notes, "Quadrupedalism would never have been abandoned if substantial distances had to be covered, especially if such journeys involved exposure to predators" (125). Easy terrestrial movement and escape from predation in apes requires the rapid movement of quadrupedal locomotion. It biped faces substantial disadvantages in these respects. This means that a greater reliance on bipedal locomotion would has required both a small home range and easy access to trees. This idea is a 180 degree shift from the Darwinian model of bipedal origins, in which upright posture was a reflection of the challenges of a poor habitat and the need to forage over long distances. Here, it is safe "secure and a rich environment" that is essential to the origin of bipedalism. In Kingdon's view, living apes naturally pursue a number of hand manipulation skills, social interactions, gestural communication, and carrying objects that require them to "squat, lie down, stand on two legs, or become three-legged" (125). For all of these behaviors, bipedal locomotion might well be naturally advantageous. But chimpanzees and gorillas cannot abandon quadrupedal locomotion and its speed advantages because of their large foraging ranges and susceptibility to predation. The commitment to quadrupedalism thereby impedes the further development of manual abilities that apes already have.

This idea provides a slightly different answer from Jolly might have given concerning why geladas are not more hominid-like than they are. Although the foraging style of manipulating small hard seeds and other objects might have been similar between early hominids and geladas, the habitat is very different. Geladas must retains an effective adaptation to quadrupedalism because they do not limit their foraging to areas where trees are readily accessible. Nor do they already show the range of manipulative behaviors shared by apes, which provided further incentives to bipedalism in early hominids.

The thrust from squatting

The squat-feeding model encompasses several untested predictions, which might well provide fertile ground for research. First, this pattern of adaptation should direct attention to the anatomy of the back. In particular, to conserve energy and maximize the use of a single foraging location, the spine should be well adapted to a bright posture, flexible in side to side movements, and capable of providing a stable platform for a wide range of movement for the arms. This may help to answer the question of why early hominids had relatively long spines, and especially in contrast with very short lumbar spines in other living hominoids. It also allows the side-to-side twisting motion of the pelvis during bipedal gait to be examined as an exaptation based on an earlier ability to rotate the upper trunk against a stationary pelvis. Normal arm-swinging upright walking depends on this flexibility of the lower spine, which would appear to be absent from living chimpanzees and gorillas, in which the flat iliac blades and the lower rib cage are strongly connected and relatively inflexible. Kingdon describes the compact, inflexible trunks of living apes (127) and their disadvantages for upright walking, but he does not explore why this configuration in apes would be advantageous for the locomotor behaviors of these apes, such as climbing or knuckle-walking. This difference from hominids is worth exploring, particularly in considering the effectiveness of early hominids as climbers.

The model also places a different spin on the usual anatomical description of the changes involved in bipedalism. Generally, the shortening and broadening of the iliac blades are seen as enabling a shift in muscular action during hip extension, recruiting the gluteus maximus as an extensor of the hip instead of an abductor. Kingdon explains the shortening of the iliac blades as a way of disentangling their action from the motion of the lower trunk, creating two separate functional units. In this way, he also explains the lengthening of the lumbar spine as part of the same anatomical change. This is potentially important because the length of the lumbar spine in the common ancestor of hominids and chimpanzees is not known. If hominids descended from an ancestor with the chimpanzee-like spine, a mechanism for the expansion in length of the lumbar spine is both necessary and welcome.

One of the advantages of bipedal locomotion often cited in explanations of hominid origins is the ability to see distances over tall grass while scanning for predators. Kingdon places a different twist on this also, by suggesting that this scanning behavior was present prior to the evolution of obligate bipedalism, as the ground apes would scan for predators from a squatting position. In this way, the apes habitually made their spines as vertically erect as possible at frequent intervals, and simultaneously required effective side to side head movement. This kind of behavior may have underlain the anterior placement of the foramen magnum and the reconfiguration of the head-spine articulation. This hypothesis would especially be interesting if it were shown that the anterior placement of the foramen magnum significantly predated the origin of the pelvic specializations for bipedalism. This kind of evidence might already be present in Sahelanthropus, Orrorin, or Ardipithecus. Especially in Sahelanthropus, where Brunet and colleagues (2002) have argued for an anterior foramen magnum, and in the Aramis occiput, where the foramen magnum also appears to be relatively anterior. Pelvic evidence is not yet available from any early hominid, and although the Orrorin femora are consistent with the weight-transmission characteristics of later hominids, it is not clear that this anatomical element is necessarily reflective of an entire pelvic anatomical complex.

One might argue that every hypothesis to explain the origin of bipedalism is in some sense an umbrella hypothesis (Langdon 1997), and this is no exception. While the fundamental change hypothesized by the model is a change in foraging strategies, this change is proposed have several effects on other elements of early hominid behavior.

The first of these involves the dynamics of hominid groups. Kingdon speculates that terrestrial life would have involved new adaptations to resist a greater diversity of predators and competitors. This adaptation would likely have involved group coordination with intimidation displays. In particular, a restriction to relatively small home ranges would of reduced the possibility of simply moving on as a response to competition or predation. Climbing would have remained very important in predator avoidance, but it arguably would not be enough to cope with the eastern African ecology.

Speciation among the early hominids

Another consequence adduced by Kingdon is on the pattern of speciation of subsequent hominid lineages after the hominid-chimpanzee divergence. Kingdon describes many of the land areas bordering on the East African coastal forest, along with the prospects for ancestral hominids occupying and spreading among these different areas. He raises an interesting point about the Zambezi basin, which is largely open grassland with extensive floodplains and gallery forests and would therefore have been ideal hominid habitat despite the present lack of hominid fossils from the area.

As Kingdon describes each African region, he makes four basic points. First, the linear movement of ground apes along the coast and into the upland regions would have placed hominid populations at such distance from each other to radically restrict gene flow between them. Second, each of the areas, ranging from the Ethiopian highlands to the Zambesi basin would have presented unique ecological circumstances that would have demanded local adaptations on the part of the early ground apes. And third, the likely habitat of the ground apes extended along river courses. This means that the apes were likely not separated by the river drainages themselves, especially since many of them are highly seasonal, but instead they were separated by the interim habitats that were highly risky and resource-poor for a woodland-dependant ape. Last, the home ranges of the ground apes were probably small, again reducing the possibility of long-range dispersal and contact among populations.

I repeated the term "ground ape" repeatedly in the previous paragraph in reflection of Kingdon's other major assumption. He promotes the ground ape as a genuine stage in the evolution of the hominids. In other words, these apes once differentiated from chimpanzees were themselves highly successful occupants of the East African forest, and could themselves spread into adjacent habitats. All this occurred before the advent of of bipedalism as reflected in later hominids. This would imply that a substantial diversity of ground apes may have once existed, on the hominid lineage, but not themselves obligate bipeds. Kingdon suggests that known fossil samples like Orrorin or Ardipithecus might in fact represent a ground ape in this sense rather than bipedal hominids.

I am unconvinced by the idea that the squatting ground ape lived for a long period of time before evolving the adaptations to effective bipedality. Indeed, Kingdon's argument about the advantages of bipedalism would seem to suggest that it would emerge quickly if the opposing need for quadrupedal locomotion decreased. The idea that the ground ape stage lasted for a long time ignores the likelihood of competition from more effectively arboreal forms.

The biogeographic separation of hominid ancestors from chimpanzee ancestors (and gorilla ancestors) creates a set of interesting problems that Kingdon doesn't address. For example, if the apes on both sides of the East African arid strip were initially the same, did this original ape form survive for some time alongside the new ground apes? Or was that form itself a ground ape (as speculated below). Did this ancestral species survive alongside its bipedal descendants for some period of time? If Kingdon's idea about widespread diversification and long survival of the ground apes were true, then these apes must have coexisted for some long time with their bipedal descendants, especially if the ground apes had significant local adaptations to different African regions.

While Kingdon does support his argument that the early ground apes would have differentiated into different species with several assumptions, I found this unconvincing. Consider that chimpanzees are spread across over three thousand miles of West and Central Africa with clear evidence of recurrent gene flow among different subspecies over the past million years or more. Lowland gorillas also have an impressive geographic range, and orangutans today comprise two long-lasting geographic subspecies, which in the past must have extended to a greater diversity on the Asian mainland as well as across the Sunda shelf. The phylogenetic pattern represented by today's great apes indicates widespread species with highly conservative ecological adaptations. This allows subspecies to remain ecologically similar for long periods of time, and enables the exchange of genes long after the initial establishment of geographically distant (or periodically isolated) populations.

Kingdon does not consider this pattern, but his argument would indicate that the ground apes (or early hominids) diverged from the phylogenetic tendencies of other ape species because of their restricted home ranges and more intensive ecological exploitation of local environments. This hinges on the idea that bipedality really doesn't increase mobility, but instead radically decreases it.

But this argument fails to recognize the energetic consequences of bipedalism after it originates. It may be true that the initial transition to bipedalism would not be possible without the means of abandoning the dependence on quadrupedal movement in foraging and flight. It may also be true that obligate bipeds continued to be at a disadvantage compared to quadrupeds in predator avoidance and daily range. But the movement of bipeds over long distances would if anything have been less costly than that of a quadruped of the same size. And the social correlates of bipedality that Kingdon notes would seem likely to increase dispersal rather than decrease it. That is to say, despite a smaller home range, more cohesive groups with potentially larger group sizes present a higher chance of significant disparities in resource access among groups, a greater variance in group sizes, increased challenges for individuals integrating into new groups, and greater incentives to colonize and disperse over long distances. Bipeds are well equipped to move along linear habitats like gallery forests, and might have done so with maximum energetic efficiency in response to resource challenges or seasonal scarcity. An increased tolerance for higher population densities would have enabled an effective migration strategy in regions where seasonal resource shortfalls in one area may have been supplemented by movement to other areas with enough to go around.

This cuts to the nature of what it is to be a biped. Once the bipedal strategy arose, did it enable greater mobility or not? Were hominid groups highly territorial, and highly sedentary, or were they instead highly mobile? Did hominids tolerate local aggregations of multiple groups, or were they committed instead to intergroup conflict? This is where a chimpanzee model potentially misleads, since chimpanzees are both mobile and territorial, intolerant of contact with neighbors and capable of long-distance dispersal for maturing females. How would bipedalism change a chimpanzee's behaviors? An unanswered question.

Unanswered questions

An unanswered question is to what extent the focus on ground-accessible foods would have precluded the use of canopy foods. As Kingdon notes, canopy fruits are the major food source for chimpanzees today. Presumably, a greater adaptation to terrestrial life including bipedal locomotion would have greatly restricted the ability of early hominids to climb into the forest canopy and exploit fruiting trees. It seems possible that competition from other primates, such as cercopithecoid monkeys, might have precluded the effective dependence on a canopy resources anyway. But this line of inquiry needs to be developed further.

Another unanswered question involves the body proportions of early hominids. Australopithecines were exceptionally short compared to living humans. And there legs were hardly longer than similar-sized apes. These legs were very inefficient for bipedal movement compared to the long legs of subsequent hominids. But one possibility is that australopithecine legs may have been effectively adapted to a squatting posture. As far as I know, this hypothesis remains to be tested. Certainly if Kingdon is right about the small foraging ranges
of early hominids, the energetic disadvantages of short legs may have been relatively minor, because hominids would never have walked very far anyway. In this respect, even the home ranges of chimpanzees would be a poor model for the relatively small home ranges of early hominids. While anthropologists have tended to contrast australopithecines with early humans, who were believed to have had larger home ranges on the scale of those occupied by living hunter gatherers, it remains possible that australopithecine home ranges were smaller even than has usually been assumed.

And of course the biggest unanswered question appeared in the form of a key fossil shortly after the book must have been finished. What about Sahelanthropus? If Sahelanthropus was in fact on the hominid lineage, then it would seem to reject the model of differentiation proposed by Kingdon--Chad is a long way from the East African coastal forest. Conversely, if it is not on the hominid lineage, its importance to the model depends on what it is. If it is ancestral to hominids or to chimpanzees or gorillas, then it potentially informs us as to the anatomy of the common ancestor to these species. If so, that ancestor may have been substantially more ground ape-like than even Kingdon might have expected, at least if Brunet and colleagues (2002) are right about the foramen magnum placement and its implications for vertical posture. One might even envisage the hypothesis that chimpanzees and gorillas themselves are substantially derived from the common ancestor because they colonized the West and Central African equatorial forests long after the common ancestor lived (although presumably before the separation of chimpanzees and bonobos). This is a lot of mileage out of one fossil sample, but the absence of a fossil record for either chimpanzees or gorillas invites speculation.


Brunet M, Guy F, Pilbeam D, Mackaye HT, Likius A, Ahounta D, Beauvillain A, Blondel C, Bocherens H, Boisserie JR, De Bonis L, Coppens Y, Dejax J, Denys C, Duringer P, Eisenmann V, Fanone G, Fronty P, Geraads D, Lehmann T, Lihoreau F, Louchart A, Mahamat A, Merceron G, Mouchelin G, Otero O, Campomanes PP, Ponce de Leon M, Rage JC, Sapanet M, Schuster M, Sudre J, Tassy P, Valentin X, Vignaud P, Viriot L, Zazzo A, Zollikofer C. 2002. A new hominid from the Upper Miocene of Chad, Central Africa. Nature 418:145151.

Kingdon J. 2003. Lowly origin: Where, when, and why our ancestors first stood up. Princeton, NJ: Princeton University Press.

Langdon JH. 1997. Umbrella hypotheses and parsimony in human evolution: A critique of the Aquatic Ape Hypothesis. J Hum Evol 33:479494.