bipedalism

Elizabeth Pennisi has a short piece in Science describing David Carrier's ideas about leg length and fighting in early hominids.

David Carrier, a comparative physiologist at the University of Utah in Salt Lake City, has jumped into the fray with a provocative idea about Lucy's legs. In earlier studies with dogs, he had found that short legs provide mechanical benefits during fights. Pit bulls' short limbs, for example, aid stability and are tough enough to sustain attack without breaking.

Carrier contends that Lucy and other australopithecines also had bodies built for defense against each other: Their short legs may have provided a competitive edge when males battled rival suitors.

This is basically the wrestler vs. distance runner physique story. And it could be true -- but is it a primary cause or a secondary one? Depends how they were fighting, I should think.

The interesting part is that it is not an argument based on optimal energy expenditure. But is it safe to use sexual dimorphism as a proxy for male competition? And were australopithecines really very sexually dimorphic?

Boy, there sure seem to be a lot of unknowns lately.

References:

Pennisi E. 2006. Was Lucy's a fighting family? Look at her legs. Science 311:330. Full text (subscription)

The current (February 2006) issue of AJPA carries an article by Craig Stanford describing the context of bipedal posture for chimpanzees in the Bwindi Impenetrable National Park. When considering how bipedal locomotion evolved in early hominids, it is an essential comparison how chimpanzees (or other hominoids) use bipedal postures. Stanford writes:

As Hunt (1994, 1996) pointed out, hypotheses for the advent of bipedalism that involve behaviors in which prehominids may have frequently engaged offer the most plausible explanations for the adaptive shift from quadrupedal to bipedal posture (Stanford 2006:225).

Stanford was able to observe a large number of episodes of bipedal posture in the study group -- 179 cases in 247 observation hours. I find the context to be the most interesting result:

All 179 instances of bipedalism were recorded while chimpanzees were foraging in large trees. All but one instance occurred as postural rather than locomotor bipedalism, and 96% of all instances occurred in a feeding context....Chimpanzees appeared to forage bipedally most often when feeding in the upper portion of the crown, reaching up to branches emergent in the sunlight, and perhaps containing harder-to-reach ripe fruit. (Stanford 2006:227).

Studies of bipedal posture in wild chimpanzees have been rare, as Stanford reviews, but have typically found fewer instances of bipedality and have included some terrestrial cases. The key finding of all studies appears to be that foraging for fruit is the main reason why chimpanzees occasionally stand.

What do the chimpanzees tell us about early hominids? Here is the suggestion:

The behavior of wild chimpanzees suggests that several aspects of the positional behavior of earliest hominids may have been given less attention that they merit. First, arboreal bipedal posture is not dichotomous with arboreal quadrupedal posture. Bwindi chimpanzees moved fluidly between four-legged, three-legged, and two-legged postures while feeding in tree crowns. Their use of three-dimensional space in tree tops incorporated elements of positional behavior most often seen as binary states. This fluid quadrupedal-bipedal shifting may have occurred in the earliest hominids as well. Arguments about whether early hominids were fully adapted to bipedal walking, or facultatively arboreal, have been carried on for at least three decades (Susman et al., 1984; Lovejoy, 1988). Recent evidence suggests that knuckle-walking may have been employed by the immediate ancestors of the australopithecines (Richmond and Strait, 2000). Chimpanzee bipedal behavior suggests that early hominids likely engaged in a fluid variety of positional behaviors and postures, but provides little evidence for the adaptive advantage of terrestrial knuckle-walking in the last common ancestor of apes and humans (Stanford 2006:230).

Now, humans are fully adapted to bipedal walking, and we are facultatively arboreal (that is, we can climb trees), so there is no reason to think that early hominids were less facultatively arboreal than we are, and I would venture that they were probably a good deal more so.

The fundamental question about early hominids is why they abandoned the ability to be facultative quadrupeds. That is something that chimpanzee positional behavior isn't going to tell us -- after all, chimpanzees take on bipedal posture in ways that don't compromise their quadrupedal abilities.

The chief importance of the chimpanzee comparison is to illustrate the kinds of ways that locomotor diversity occur in hominoids. After a brief discussion of locomotor flexibility in gorillas, Stanford concludes with this:

Rose (1984) argued that there is no reason to view the origin of bipedalism as a progression from "poor biped" to "good biped." Instead, there was likely a diversity of forms of bipedalism in the earliest hominids. One such hominoid example may be Oreopithecus bambolii, a sup-
posed bipedal ape (Kohler and Moya-Sola, 1997). The bipedal evidence from Bwindi, Mahale, and Gombe supports this view of early hominid evolution. Instead of viewing the earliest bipedal adaptation as the lowest
rung on a posture/locomotion evolutionary ladder, it may be that early hominid species evolved a variety of forms of bipedalism in particular ecological contexts (Stanford 2006:230).

I guess that is one possibility to explain evidence of vertical posture in early hominids in the absence of good evidence of bipedality (from postcranial evidence).

The "diversity of forms" argument really suggests a stage during early hominid evolution when the ability to be effective quadrupeds had not yet been lost. Perhaps we will find these quadrupedal hominids. Perhaps we already have. On the other hand, this idea opposes the hypothesis that locomotor evolution may have either caused the origin of the hominid lineage or very closely followed it.

It seems to me that the level of species diversity of early hominids and this locomotor problem may be strongly linked. But I think they might be linked in the opposite direction than one might assume.

Suppose, for instance, that the hominid lineage arose as an adaptive radiation resulting from a significant new adaptation for bipedality. The "adaptive radiation" would be the origin of many new bipedal species spreading and adapting to different ecologies. Early hominid species diversity would be a consequence of their novel locomotor adaptation.

In contrast, if hominids originated as one among many quadrupedal apes in the Late Miocene, they might well have adapted over a long time as quadrupeds within a single ecology to which they remained limited. Perhaps the attainment effective bipedality would have spurred an adaptive radiation, but this event would have followed long after the origin of the hominids. Hominid species diversity might have always been low, or might have remained low until the Late Pliocene.

Now I don't think any of these arguments can be taken very far. It is always possible that bipedality arose early without any consequent adaptive radiation, or that there were multiple bipedal ape lineages other than hominids, or almost any other combination of events. There just isn't fossil evidence that could delimit hypotheses about hominid origins.

But I can't think about diversity without considering the mechanisms for it to have arisen. And while it is possible that many hominoid lineages were experimenting with bipedal posture and locomotion in diverse ways, I can't think of what would have caused the diversification of a large array of hominid species in the absence of bipedality.

References:

Stanford CB. 2006. Arboreal bipedalism in wild chimpanzees: Implications for the evolution of hominid posture and locomotion. Am J Phys Anthropol 129:225-231. Abstract

The BBC is running this article about a new study that evaluates the bipedality of A. afarensis using robotic design software:

Now, a team of scientists from around the UK have used computer robotic techniques to work out the most energy efficient gait for afarensis based on Lucy's skeleton and the Laetoli footprint trails.

They claim to have cleared up the debate by finding that, based on their model, Lucy almost certainly did walk tall.

There has been a long-standing debate about how human Lucy was
"Assuming that the early human relative Australopithecus afarensis was the maker of the Laetoli footprint trails, our study suggests that by 3.5 million years ago at least some of our early relatives - despite their small stature - could sustain efficient bipedal walking at absolute speeds within the range shown by modern humans," co-author Weijie Wang, from Dundee University, told the Scotsman newspaper.

So what we seem to have here is a computer software equivalent of early 1980's science. Perhaps they programmed Owen Lovejoy?

The paper (abstract) is a little more interesting than the BBC description. It does a kind of optimization modeling to find the speed and style of locomotion with the lowest energy cost. That lowest-cost speed was associated with a human-like gait at around 1 meter per second (m/s). Here is the logic:

Rather than trying to interpret the behaviour of such species by a combination of analogies to humans in certain anatomical regions with analogies to other apes elsewhere, it seems sensible to adopt a reverse-engineering approach and determine what kind of locomotion a particular set of body proportions were best 'designed' to perform. Since the locomotor system is concerned primarily with the application of external force by the body, simulation techniques drawn from mechanical engineering are a potential means of predicting the significance of differences in proportions for the motion and force characteristics of bipedal locomotion (Sellers et al. 2005: 2).

The authors relate their gait findings to the preserved Laetoli footprint trails, and find something very interesting. The trails have footprints that are very close together -- especially for the larger, possibly dual G2 trail. This has previously been interpreted as meaning that the walking speed of the larger individual who made this trail was very slow (Alexander 1984; Charteris et al. 1984) -- only around 0.7 - 0.8 m/s. The model in this study predicts a faster speed of around 1 m/s, which would be close to the optimal walking speed estimated for Lucy's proportions.

They do not address a relevant question, which is whether the larger trail was made by an individual larger than Lucy, who might have had a different optimal walking speed. Indeed, there is a basic assumption of monomorphism. It is partly covered by the fact that living people don't exceed 1.0 m/s for their average walking speed by very much, so the variation between large and small A. afarensis individuals may have been slight. The basic finding seems to be that shorter legs have an optimum gait that involves more, slightly shorter, steps, while longer legs take fewer steps more slowly. This isn't surprising based on a pendular model: shorter pendula have shorter periods, and longer steps with a shorter leg must require more energy-wasting up-and-down motion.

An important weakness of the model is that it considers costs only due to motion in two dimensions: forward and up-and-down. The wide pelvis of A. afarensis might be expected to exert greater costs in a side-to-side dimension compared to recent humans, and that energy effect is not considered.

But the bottom line:

Thus, within the limits of our model, and assuming that Taylor and Rowntree's (1973) data are reliable, the bipedal performance of Australopithecus afarensis, as predicted by our model is not only much closer to that of modern humans than to that of bipedally walking great apes, but at normal walking speeds, shows a clear speed/cost advantage over chimpanzee quadrupedalism. Climbing remains significantly more energetically expensive than terrestrial quadrupedalism for chimpanzees, despite their musculoskeletal adaptations (Pontzer and Wrangham 2004). Pontzer and Wrangham (2004) have shown that the costs of locomotion in chimpanzees are nevertheless dominated by terrestrial walking, because of very high daily travel distances, versus only limited use of climbing. If we make the major (and quite likely incorrect) assumption that the African apes existing at the time of A. afarensis were ecologically, morphologically and physiologically similar to modern common chimpanzees, then our data would tend to support Rodman and McHenry's (1980) argument that the adoption of bipedalism offered energetic advantages to early human ancestors (ibid., 9).

In any event, it won't quiet doubters:

However, Professor [Christopher] Stringer believes the controversy will not vanish overnight.

"There are still some people who argue that, looking at the anatomy of the foot bones of afarensis, that they were unlikely to have made the Laetoli footprints," he told the BBC News website.

"So it doesn't end the argument because there is still the possibility that there were different creatures around at the time."

No doubt soon, Kent State will have a droid afarensis army to finally crush this dissent and bring order to the galaxy.

References:

Sellers WI, Cain GM, Wang W, and Crompton RH. 2005. Stride lengths, speed and energy costs in walking of Australopithecus afarensis: using evolutionary robotics to predict locomotion of early human ancestors. Roy Soc Interface Online

Caley Orr (Personal page, Arizona State University) has an advance paper in AJPA examining convergent features in the wrists of knuckle-walking hominoids and the terrestrial giant anteater (Myrmecophaga tridactyla). Did you know that some anteaters were knuckle walkers? I certainly didn't, until I read this!

The background for this paper is the recent finding of certain features in the wrists of early hominids, specifically the distal radius of Australopithecus afarensis and Australopithecus anamensis, that appears similar to those found in chimpanzees and gorillas (Richmond et al. 2001). It has been argued that these features are primitive retentions from a knuckle-walking ancestor, a hypothesis viewed as consistent with the idea that all of the African apes descend from a single agent knuckle-walking species. The current paper gives a good synopsis of this evolutionary problem, including the alternative hypothesis that knuckle-walking evolved in parallel in the chimpanzee and gorilla lineages, so that the hominids did not descend from an age in knuckle-walker.

So why study anteaters? The idea is that different phylogenetics lineage that share a behavior ought to share convergent features to support that behavior. African apes have long fingers for suspensory climbing, which are talked out of the way for quadrupedal movement, hence walking on the knuckles. Giant anteaters have long claws for digging into insect colonies, and these long claws are talked out of the way for a quadrupedal walking. Thus the purpose of this study was:

1. To determine if the locomotion and hand postures of the giant anteater are appropriately analogous to the knuckle-walking of African apes;

2. To identify features of the Myrmecophaga hand and wrist that converge functionally with Pan and Gorilla, and that distinguish these taxa from their non knuckle-walking out groups and terrestrially digitigrade primates; and

3. Through the above analyses, to help determine the traits most likely to be adaptive to knuckle-walking, thereby suggesting which features of the early hominin and modern human wrists might be reliably indicative of a knuckle-walking ancestry (Orr 2005:3).

Did it work? The study did find some features of giant anteaters that made their wrists similar to those of chimpanzees and gorillas. But does this provide support for the idea that early hominids were descended from knuckle-walkers? Orr saves a critical piece of logic for the discussion:

A convergence study can only provide positive or equivocal evidence in testing hypotheses of adaptation for purported knuckle-walking features of the African Hominidae (or any other such study). That is, because all taxonomic groups have unique evolutionary histories, a convergence test cannot truly falsify a hypothesis of an adaptation for a particular lineage. However, convergence study can provide positive support for the hypothesis that structure X is an adaptation to function F, if X distinguishes F- performing taxa from their respective non-F-performing outgroups (Orr 2005:18, emphasis in original).

OK, so we should be wary. Comparing australopithecines to anteaters cannot falsify the hypothesis that hominids had knuckle-walking ancestors. In other words, it is not testing any hypothesis of human origins, although it may provide evidence consistent with one or more of them. Here's the summary of anteater-hominid resemblances:

Morphological features that appear in the hominin lineage shared by Myrmecophaga, Pan, and Gorilla, to the exclusion of their respective outgroups and digitigrade primates, are supported as adaptations to knuckle-walking and provide strong inference of a knuckle-walking last common ancestor (LCA) of Gorilla, Pan, and hominins. Only one such feature (proximal expansion of the non articular surface of the dorsal capitate) appears in the hominin lineage. Human capitates show the African apes state of proximal expansion, and the A. afarensis capitate (AL 333-40) shares the morphology of Gorilla, Pan, and Homo (Orr 2005:19).

Orr discusses the distal radius articular ridge that features in the arguments of Richmond and colleagues (2001), but does not designate this trait as one that necessarily reflects knuckle-walking as opposed to other kinds of vertical hand posture during locomotion, as found in cercopithecid monkeys.

If you're interested in the origins of knuckle-walking, and the question of whether early hominids were knuckle-walkers, this article is for you. As for myself, I think the issue is more likely to be settled with more fossil evidence of Miocene apes and their locomotor styles, rather than the examination of other mammalian lineages. It remains a mystery to me why early hominids should retain features useful only for a knuckle-walking, when their knuckles clearly could not have reached the ground. It seems more likely to me that there is some other function for which these characters might be adaptive related to early hominid locomotion, such as climbing, or other activities. Phylogenetic inertia is never very convincing, especially for early hominids, says they altered almost every other interface between their body and the environment in the pursuit of more perfect bipedal locomotion.

References:

Orr CM. 2005. Knuckle-walking anteater: a convergence test of adaptation for purported knuckle-walking features of African Hominidae. Am J Phys Anthropol (advance before print).

Richmond BG, Begun DR, Strait DS. 2001. Origin of human bipedalism: The knuckle-walking hypothesis revisited. Yrbk Phys Anthropol 44:70-105.

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.

References:

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 418:145Ð151.

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 33:479Ð494.

The most dramatic illustration of bipedalism is the pelvis, and the most dramatic specimen demonstrating pelvic morphology is the relatively complete skeleton from Hadar, Lucy, AL 288-1. This important fossil preserves a nearly complete innominate (hip) bone and sacrum, which have been used to reconstruct the pelvis of this individual. The upper portion of the innominate bone, called the ilium, is short and curving compared to the long, flattened ilium of chimpanzees and other apes. This curvature provides an anterior attachment for the muscles that pull the femur forward during walking or running. Although the ilia are short in length compared to a chimpanzee, they extend more broadly to the side, resulting in a pelvis that is very broad overall. Indeed, this pelvis is nearly as wide as that of a human female, despite the small body size of the australopithecine. This pelvic width contributes to a very different body shape for early hominids than for humans.

The width of the pelvis affects the muscular requirements of walking. Whenever one leg supports the body, the trunk of hominids tends to fall away from the supporting leg. The muscles that prevent the body from falling over attach to the lateral part of the ilium and to the femur, pulling the trunk upward around the hip joint. A wide ilium tends to increase the efficiency of these muscles. Their effectiveness is also aided by a long femur neck, just as long handles on a pair of scissors greatly increase the force with which they can cut. This configuration of muscles is similar to the condition found in living people, but it is much more extreme. In living people, the pelvis is much narrower in proportion to overall body height, and femur necks are much shorter in proportion to femur length.

A number of hypotheses compete to explain why the bipedal adaptation of early hominids should be different from modern human bipedalism in this way. One explanation is that the pelvic width contributes to the length of the stride, by rotation of the pelvis during walking. This rotation would increase stride length without increasing the length of the swing of the legs, allowing an increased stride without lowering the mass of the body--which if lowered would subsequently have to be raised again through greater muscular exertion (Rak 1991). Alternatively, the widely spaced femora may allow a greater mechanical advantage for the muscles that draw the legs medially, toward the midline. Such a configuration would be advantageous for certain leg motions, especially the style of climbing that requires the legs to clamp around a branch or trunk. This kind of climbing would be more necessary to bipeds who lacked the prehensile feet of living apes.

The wide pelvis of early hominids had one consequence beyond those related to bipedalism, by setting the stage for a major evolution of the birth process. During birth, the infant must pass through the birth canal, entering it through the pelvic inlet. Although relatively small compared to the pelvic inlets of the apes, the oval shape of the australopithecine pelvic inlet probably did not create any problems during birth because australopithecine infants likely had head sizes about the same as those of chimpanzees. Even so, Robert Tague and Owen Lovejoy (1986) have speculated that birth in australopithecines may have involved a more complex series of events than chimpanzee births, with the possibility that the infant head may have had to rotate a quarter-turn to be born in line with the sideways oval in a manner similar to the half-rotation of a human infant during birth. Karen Rosenberg and Wenda Trevathan (2002) suggest that at this time, hominid females began to require assistance with the birthing process. The pelvic constraints associated with bipedal locomotion would come to determine much more about the birth process in later hominids.

More on bipedalism in hominids

References:

Rak Y. 1991. Lucy's pelvic anatomy: its role in bipedal gait. J Hum Evol 20:283-290.

Rosenberg KR, Trevathan W. 1996. Bipedalism and human birth: the obstetrical dilemma revisited. Evol Anthropol 4:161-168.

Tague R, Lovejoy C. 1986. The obstetric pelvis of A.L. 288-1 (Lucy). J Hum Evol 15:237-255.

The skeletal adaptation to bipedalism is well documented in early hominids. What is less clear is what events led to this adaptation and its eventual success. Hypotheses about why bipedalism arose have been very common, but most lack the necessary evidence to test them. All apes can walk bipedally, so the behavior itself was within the capabilities of the common ancestors of hominids and chimpanzees. What is necessary is to explain how bipedalism became so essential that it provoked skeletal adaptations that made other forms of locomotion much more difficult.

One argument is efficiency. Human bipedalism is very efficient at normal walking speeds, because forward motion results from gravity swinging each leg forward like a pendulum. The walking biped recaptures this forward momentum by slowing the swinging leg before footfall. As a result, walking at normal speeds on level surfaces requires very little muscular activity, making bipedalism more efficient than knuckle-walking or quadrupedalism (McNeill Alexander 1985). Aside from its energetic efficiency, bipedalism also has the advantages of raising the head, and therefore allowing a wider range of vision in a grassland environment, and of freeing the hands for carrying items or for tool use.

Despite these advantages, bipedalism also has considerable disadvantages. The first is that it makes climbing considerably more difficult. Without the ability to grasp with the feet, hominids are less secure in an arboreal setting. There are many indications that climbing remained an important part of the behavior of early hominids, discussed below. The combination of features found in early hominids reflects a compromise adaptation to climbing, which is based on the presence of morphological adaptations to bipedalism in the pelvis and foot. Part of this compromise was structural, involving much more powerful arms and possibly human-proportioned hands for gripping branches rather than suspending from them. Another part of the compromise was behavioral. The loss of a grasping foot is also a serious problem for child-rearing. In chimpanzees and other primates, the young can use their hands and feet to grasp and cling to their mother's fur. For hominid infants, such clinging would have been much more difficult, if not entirely impossible. One of the adaptations to bipedalism must, then, have been a behavioral change toward carrying dependent offspring until they were old enough to walk.

Over time, scientists have devised many different theories to reconstruct the circumstances that led to the evolution of bipedalism. Charles Darwin himself correctly assumed that the African apes are the closest human relatives, and constructed a model for hominid origins that stressed the appearance of bipedalism from an ape-like ancestor. In Darwin's model, bipedalism is seen as the adaptation resulting when a quadrupedal ape is forced to assume a terrestrial adaptation. In Darwin's formulation, this adaptation was partly caused by the advent of a hunting subsistence pattern, where the hands needed to be free to carry weapons and meat. Additionally, Darwin thought that a change in habitat from woodland to savanna left early hominids without the refuge of trees, resulting in less importance of climbing and a greater need for efficient movement on the ground. Other later researchers picked up many of the themes of Darwin's model, stressing other important features of life on the savanna, such as the need to see over tall grass, and the need to adapt to intense solar radiation. Bipedalism has been suggested as an adaptation to both these factors, by placing the head high and upright, and decreasing the exposure of the trunk to direct light from overhead. This model came to be called the savanna model, or stressing the importance of hunting in the model, the killer-ape hypothesis.

Today, we have greater knowledge about the environments that early hominids occupied, and many aspects of the savanna model do not appear to describe the conditions under which bipedalism evolved. All of the sites before 3 million years ago seem to have been partially or fully wooded, and no early hominids are known from full savanna environments. Additionally, the fossil forelimb elements of early hominids demonstrate the continued importance of climbing. The importance of hunting has been questioned because chimpanzees hunt extensively without the adaptations of early hominids, and because no tools, weapons or adaptations to making tools are known from the earliest hominids. These observations imply that bipedalism was not the simple consequence of a single climatic change.

Lovejoy (1981) has suggested that social factors may have been principally responsible for the origin of bipedalism. In his hypothesis, food sharing was an important component of social behavior. Lovejoy speculates that males may have supplied food to females in order to gain mating access or to contribute to the parenting of their own offspring. This behavior would require the use of hands for provisioning. Such a hypothesis must be reconciled with the apparently high level of sexual dimorphism among early hominids, but may provide significant insights.

One reason for the proliferation of hypotheses to explain hominid origins is that we have almost no knowledge about the postcranial anatomy of the immediate ancestors of the hominids. Most hypotheses have assumed that the common ancestors of living African apes and hominids were essentially like chimpanzees, with suspensory locomotion in the trees and knuckle-walking on the ground. Whether hominids originally evolved from a knuckle-walking ape or not has been controversial. Some scientists, like Brian Richmond and David Strait (2000), argue that early hominids like Lucy bear anatomical features that indicate a knuckle-walking ancestry. In this formulation, the occasional bipedal locomotion of chimpanzees and gorillas is a model for how obligate bipedalism originated. The anatomical changes that characterize the known hominid fossils grow from a more intensive use of this basic hominoid behavior.

Other scientists point to the possibility that knuckle-walking evolved in parallel in chimpanzees and gorillas. The manner of arboreal locomotion in living and extinct apes seems to have been greatly influenced by body size. Known early hominids average slightly less than chimpanzees in body size, and it is possible that their common ancestor was small, rather than chimpanzee-sized. Wolpoff (1999) has suggested that the ancestors of hominids may have been small apes who often walked or ran bipedally above large branches, as well as on the ground. From this perspective, the knuckle-walking of chimpanzees and gorillas and the bipedalism of hominids represent different strategies for ground locomotion related to body size. Under this hypothesis, the large apes developed a suspensory adaptation in response to increases in body size, with locomotion on the ground occurring later than or secondary to this increase. In contrast, early hominids adapted more fully to the ground before their body size increased, resulting in an anatomical adaptation to bipedalism, with climbing secondary.

None of the factors here excludes any of the others, and probably the origin of hominid bipedalism involved a complex combination of these and possibly others. Until scientists have more knowledge about the anatomy of the first hominids and their ancestors, we will be unable to rigorously test these hypotheses. Nevertheless, even as the record of hominid evolution has been pushed back to six million years, bipedalism remains the hallmark adaptation of our lineage. For this reason, explanations for its origin remain one of the most important parts of paleoanthropology.

Bipedalism :: legs and feet

Bipedalism :: pelvis

References:

Lovejoy CO. 1981. The origin of man. Science 211:341-350. JSTOR

McNeill Alexander Ra. 1992. Human locomotion. In: Jones S, Martin R, Pilbeam D, editors, The Cambridge encyclopedia of human evolution. Cambridge: Cambridge University Press. p 80-85.

Richmond BG, Strait DS. 2000. Evidence that humans evolved from a knuckle-walking ancestor. Nature 404:382-385. PubMed

Wolpoff M. 1999. Paleoanthropology. Second edition. New York: McGraw-Hill.