One of my more favorite reads was Aaron Filler's Upright Ape: A New Origin of the Species, shortly after it was published. The suggestion(s) regarding human evolution were attractive and revolutionary, while the discussions of homeotic mutations and their mechanisms (based upon peer-reviewed work) were enlightening and form part of the foundation of my own approach to understanding how mutation, development, and Darwinian selection work together (a subject I haven't blogged much about although it underlies much of my writing here).
Filler's primary suggestion is that the main stem lineage of the Great Apes has been walking upright since shortly after it diverged from the ancestors of the ancestors of the gibbons and siamangs due to a homeotic mutation that modified the spine to give it the potential to support an upright stance for long periods, something the gibbons and siamangs lack. (Although they can and do walk upright, both in the canopy and on the ground.) One of the implications of this theory is that the common ancestor of humans, gorillas, chimpanzees, and bonobos walked upright, and that knuckle-walking behavior evolved independently in the lineage leading to gorillas from that leading to chimpanzees and bonobos.
Figure 1: Example of the detailed anatomical discussion of the proposed homeotic mutation that lead to the human/great ape backbone structure. Click on image to see illustration and caption at the book's website. (From Reference 3, figure 9-5.)
Now, in the advance online Early Edition of PNAS, we find Independent evolution of knuckle-walking in African apes shows that humans did not evolve from a knuckle-walking ancestor (by Tracy L. Kivell and Daniel Schmitt), unfortunately behind a paywall, that describes research thoroughly undermining the notion that humans evolved from a knuckle-walking ancestor. Let's look at the research first: ...
What Kivell and Schmitt did was examine the "features most commonly thought to reflect knucklewalking behavior in the African ape wrist", in terms of their occurrence and development in many primates, and especially gorillas as well as chimpanzees and bonobos. They found "(i) that most gorillas lack key features that have been assumed to be critical for limiting extension of the wrist during knuckle-walking ([refs]), and (ii) these features are found in monkeys that use a variety of different hand postures and substrates."
Assuming that such features are necessary (or highly desirable) for knuckle-walking, we should find them emphasized in gorillas, and at earlier ages, since gorillas are larger, thus putting more stress on the bones of their hands during knuckle-walking, and normally start earlier during development. Instead:
In addition, the ontogenetic analysis shows that the features of the scaphoid that are assumed to be essential for knuckle-walking ([refs]) are not only inconsistently developed in Gorilla, but, when present, do not appear relatively earlier in development in gorillas (Table 2). Therefore, using the traditional functional interpretation of these features ([ref]), it would appear that the Gorilla radiocarpal joint may be actually less, rather than more, stable in extension throughout ontogeny compared to Pan.The mention of stability during extension of the radiocarpal joint (bending back the wrist) leads to the next important feature of this report: the proposal that the method of knuckle-walking used by gorillas is different from that of chimpanzees and bonobos.
We propose that Gorilla uses a relative ‘‘columnar’’ forelimb posture during knuckle-walking in which the hand and wrist joints are aligned in a relatively straight, neutral posture compared to the more extended postures adopted by Pan (Fig. 3). Animals using a relatively columnar wrist and hand posture would have carpal joints that are in line with the hand and forearm, similar to limb joint position in large graviportal animals such as elephants ([ref]). Supporting loads directly over more vertically-oriented forelimb joints during support phase explains the absence of posited bony adaptations to bending loads in gorillas and also permits more mobility at the joint ([ref]). By contrast, Pan, which exhibit extended wrist postures (Fig. 3), will experience higher bending loads. Thus Pan carpal bones have relatively prominent osteological features that have traditionally, but mistakenly, been interpreted simply as features associated with knuckle-walking in general rather than with a specific posture. The notion that Pan and Gorilla use different wrist postures is consistent with the morphometric data presented here. Although this hypothesis has yet to be explored in detail with videographic data, this idea is further supported by previous research showing that Gorilla exhibits increased wrist mobility compared to Pan ([ref]), a more hyperextended elbow joint ([ref]) and relatively equal length of rays 2 through 4, which creates a larger, more stable area over which to disperse axial loads ([ref]).Imagine the difference between doing push-ups on your fists and on a steel bar you've got your hand wrapped around with your wrist bent back. This is sort of what the difference is, but only sort of. Unfortunately, their "figure 3" is behind a paywall, but the important takeaway is that there is a difference in mechanism, the details of that difference, while important, aren't necessary to the wider implications.
Kivell and Schmitt have provided very strong support for the idea that knuckle-walking works differently, is used differently, and probably evolved independently in these two lineages. A less technically oriented discussion (than the paper) is provided by Science Daily, I'm not going to try to replicate their work. (afarensis, FCD is not really convinced, I've discussed Filler's theory in comments on his (old) blog, and I've expanded and modified some of my arguments there in this post.)
Support for the Upright Ape
Instead, I'm going to discuss how this new research relates to the "Upright Ape" hypothesis. One key hypothesis here is that the homeotic mutation to the spine "pre-adapted" it to support the upper body when standing, walking, or running upright. I won't go into the details, but with this adaptation in place, we need to ask precisely why any possessor would go in for knuckle-walking. The answer is that the requirements of brachiation (swinging from the arms) include suppressing a twisting movement between the hips and the shoulders, a need that grows greater with greater size (mass). An ancestral "Great Ape" weighing no more than a typical gibbon might have found this movement easy to suppress, but a larger ape that depended on brachiation would have been under some selective pressure to suppress this movement.
(Another possibility, IMO, is that the lumbar structure of gibbons has actually become adapted to use the springy structures of the lumbar transverse process (LTP) to provide energy storage from/to this twising moment, which in Great apes must be suppressed by muscular action at the cost of energy. AFAIK no research has been done into this possibility. I'll mention that the springy structures involved are used in most mammals to counter the drop of the belly, allowing it to be suspended during walking and storing energy during running/leaping, while in Great apes it tends to counter the forward droop of the upper body while standing upright (because it has been moved dorsally of the center of flexion (bending) of the backbone by the homeotic mutation). For more detail, I must refer you to the book, I just don't have the expertise, and haven't done the detailed research, to attempt it. Thus I must also leave my suggestion regarding the gibbons as a possibility, until I find research (if any) into the details of how these structures work during active brachiation.)
Filler makes the case that the long hip structures and functionally short lumbar structures in African Great Apes represent adaptations to this selective pressure, and then goes on to argue that there are enough differences that this adaptation was probably made independently in chimpanzees/bonobos vs. gorillas. He also makes a persuasive case that this adaptation is responsible for making it much harder for African apes to walk upright efficiently, because they are forced to twist their body with, rather than counter to, their hips. This, then, would explain the parallel adoption of knuckle-walking by the two lineages during or after their divergence from each other and also from that leading to humans, which appear to have happened in one event (with gorillas diverging earlier from a lineage that later split to create those leading to chimps/bonobos on the one hand and humans on the other, although IMO a more complex triple split with a sustained period of reduced gene flow is more consistent with the evidence). The common ancestor was either small, made little use of brachiation, or both. After the split, both lineages developed into comparatively large-bodied brachiators, later becoming increasingly terrestrial and now dependent on knuckle-walking where the common ancestor would have used upright walking somewhat similar to that of gibbons and siamangs.
A suggestion (by Thorpe, Holder, and Crompton) that bipedalism developed among arboreal apes as "an Adaptation for Locomotion on Flexible Branches" was countered by a comment (by Begun, Richmond, and Strait) referring to the evidence of shared features indicative of knuckle-walking and appealing to parsimony as demonstrating its use in the common ancestor of humans and African apes. With this paper, we see the argument of the Begun team dissolve: There is no longer any strong evidence of knuckle-walking in the common ancestor, or any of the central lineage(s) of the great apes.
The Thorpe/Crompton team hasn't stood still, a more recent review examines a great deal of detail regarding the mechanics of locomotion, especially with respect to foot-ground contact and the movement of the center of gravity (COG), in support of an arboreal origin for bipedalism. They deal with the knuckle-walking hypothesis thus:
To our knowledge, Gebo is the only supporter of the knuckle-walking hypothesis to have offered a functional argument linking knuckle-walking and the origins of modern human bipedality, but as we have shown, his argument, which is restricted to foot function, is poorly supported by the data. No explanation appears to have been offered of how the characteristic flexed hindlimb postures of knuckle-walking gait could have been pre-adaptive for the extended hindlimb postures of modern human walking, or indeed how the transformation could have occurred. Further, the knuckle-walking hypothesis requires that orthogrady evolved twice: from pronograde simians to the orthograde crown hominoids – and then following an adoption of terrestrial knuckle-walking by the common African ape ancestor to orthograde bipedality in hominins. We prefer the alternative, that knuckle-walking evolved evolved independently in gorillines and panins, as the ontogeny of phalangeal and metacarpal scaling ([ref]) and of other 'knuckle-walking features' ([ref]) is different in panins and gorillines, suggesting that knuckle-walking evolved more than once among the African apes.Kivell and Schmitt have certainly provided great support for this preference. However, there are some problems with this latest (AFAIK) volley.
Although they mention Filler's work with homeotic mutations, Crompton et al. do not (as far as I can tell) take note of the implications of lumbar stiffening as an adaptation for brachiation in larger-bodied apes, although it seems fully consistent with their model. Apes that spent most of their time clambering around in an upright position (with little brachiation) might well have had no need for such lumbar stiffening. More importantly, Crompton et al. fail to allow for the selective advantage of the springy backbone supporting the upper body. (In fact, even Filler puts more emphasis on support standing or walking rather than running.)
Crompton et al. actually discuss the use of heel-strike in walking by various apes, and mention the "lack of heel-strike in modern hylobatids", but fail to make the connection to the shock-absorbing, and especially energy-storing capacity, of the springy lumbar structures of Great apes (including humans). Of course, I don't recall any special emphasis on this in the book, but then the Filler wasn't arguing against the Thorpe/Crompton suggestion of arboreal bipedalism. Although I can't speak as an expert, it seems to me that the advantages of the Great Ape lumbar structure would primarily apply to ground and very large branches/trunks, where the elastic support for the upper body could cushion the jarring effect of the heel-strike and store at least part of its energy. Landing on smaller branches with a heel-strike would be less problem, as they could provide the springy support, alternatively too much force could destabilize things, so the heel-strikes used by Great Apes on small branches are probably as careful as those of humans on icy pavement.
Problems with Current Selective Models
What this suggests to me is that the stem lineages of great apes relied much more on terrestrial movement than Crompton et al. suggest. Of course, reliance doesn't necessarily mean frequent use. One major problem I have with all these studies is their tacit assumption that energy efficiency, or frequent use, represent a good measure of selective advantage. Apes are social animals, which means that intra-specific competition is extrememly important in selection, both within and between social groups. The "winners" of these competitions could be expected to have as much as they needed to eat, so energy efficiency would be less important than victory. Similarly, all such competition is ultimately "life-and-death", at least reproductively, given the reproductive advantages accruing to high-status individuals, so adaptations that reduce the risk of high-risk behavior involved in such competition would likely be selectively advantageous even at the cost of efficiency, and even when the behavior involved is not frequent.
In arguing for an arboreal origin for bipedalism, Crompton et al. state:
Kingdon (2003) has proposed that in Africa, from the Middle to Late Miocene, fragmentation of closed forest alternated with reclosure and reinvasion of gallery-forest, moist-woodland and rainforest environments, changes also clearly documented by Elton (2008). Within branches of both the Pan and the Gorilla lineages, the height-range and frequency of vertical climbing locomotion must have increased, suggests Kingdon (2003), to facilitate access to preferred foods in the main and emergent canopy, while permitting travel between trees in broken-canopy woodland on the ground. Middle Miocene crown hominoids, such as Hispanopithecus (Dryopithecus) laietanus, are of a similar size range to living great apes, although undoubtedly male body weights for living great apes exceed estimated values for the Miocene. Thorpe et al. (2007a) thus speculate that the gorillines and panins, independently, became increasingly specialized on forelimb power, to sustain safety and effectiveness of increased vertical climbing, and so tended to adopt similar, extended-elbow, flexed-hip-and-knee kinematics when moving on the ground, hindlimb musculature being unable readily to sustain hip and knee extension and hence a bipedal gait. Hominin ancestors, we speculate, sacrificed continued access to the canopy, and became increasingly ground and small-tree dwellers. Lacking the increased specializations for vertical climbing, they were able to sustain a bipedal gait – and we may add, inasmuch as they were terrestrial, that they could sacrifice coronal-plane mobility, which also characterizes the orangutan, in favour of more effective parasagittal force-production.Alternatively, my best interpretation of Filler would suggest that the "gorillines and panins, independently, became increasingly specialized on" brachiation, perhaps not often but in selectively critical circumstances, producing the independent lengthening of the hip and stiffening of the lumbar region adduced by Filler, but making the ancestral bipedalism very inefficient, producing independent adaptations for knuckle-walking. "Hominin ancestors", pretty much retained the ancestral condition, which would be very Australopithecus-like. Only with the appearance of the lineage(s) called "Homo habilis" and the transition to a Homo erectus-like form do we find the more sophisticated gaits found in modern humans.
The suggestion that the ancestral "Great Apes" possessed a functional upright bipedalism pretty much identical to that of the Australopithecenes, with all the modern "Great Ape" lineages representing separate offshoots independently adapted for arboreal lifestyles at the expense of the ancestral bipedalism, is generally consistent with both Filler and the Thorpe/Crompton team. However, the issue of the relationship between heel-strike and the lumbar modifications speaks for a much greater reliance on terrestrial movement than is consistent with the Thorpe/Crompton arboreal explanations.
Although Filler didn't speak to it, I think we should consider the environmental implications: conditions were not always a closed canopy:
Mid and late Miocene African catarrhines are associated with a variety of habitats, over time as well as in different places ([refs]). Early Miocene sites such as Mfwangano Island and Songhor, sampling several catarrhine genera including Proconsul and Rangwapithecus, probably had environments containing evergreen, multi-canopied forest ([refs]). The early Miocene catarrhines radiated extensively into such arboreal habitats, filling frugivorous, folivorous, above-branch and mixed arboreal/terrestrial niches ([ref]). The slightly more recent (c. 18 Ma) Hiwegi Formation on Rusinga Island, by contrast, appears to have single-canopied, disturbed woodland, known best from a rich floral assemblage ([ref]). Unfortunately, it has no directly associated ape fossils although several taxa are known from Rusinga Island deposits of a similar age ([ref]).Given the widespread lack of fossils, we can't assume that any area lacking fossils lacked some sort of ape population. Proconsul, according to Filler, did not possess the specialized lumbar structures found in Great Apes, although a very similar species did. The "evergreen, multi-canopied forest" mentioned by Elton may well have been similar to the primary environments of both African and Asian modern Great Apes, while the "single-canopied, disturbed woodland" is another type of environment entirely. With broken canopies, and even a single canopy which would not have been completely opaque, there would have been much more undergrowth. This in turn would have led to much more scrambling and clambering moving over the ground. The "disturbed" aspect of the woodland suggests considerable downwood, placing all sorts of obstacles to overland transport. I would suggest that from the earliest expansion of the "Great Apes", that is those possessing the lumbar adaptations adduced by Filler, they specialized in rapid movement through this sort of terrain.
Figure 2: Example of "disturbance": damages of storm Kyrill in Wittgenstein, Germany. (From Wiki.)
In areas with high relief (from erosion), there wouldn't have been a clear boundary between this sort of movement and low arboreal movement through the "single-canopied, disturbed woodland". Mammals the size of Proconsul spend a lot more energy in vertical movement than horizontal,A1 so an ability to move horizontally, or as close to it as possible, through a variety of micro-landscapes would be adaptive. So would an ability to run (when necessary, see above) over hard ground and large branches/logs at similar levels. Unlike the "assisted bipedal walk" that may be the safest way to cross high bridges, bipedal running during necessary high-risk activity would probably have depended on balance. This is hardly surprising, many primates can be taught to ride a bicycle, a task demanding great balance.
Figure 3: High relief terrain, from Oregon. This is badlands, much less wooded than the type of terrain I'm discussing, but it allows you to see the relief because of the lack of vegetation. Imagine forest over this terrain, with frequent disturbance as in Figure 2. (From the files of OregonLive.com.)
Given the generally Australopithecus-like fossils being found in Africa, some evidently dating back as early, or earlier, than the best date for the split between the lineages leading to humans vs. chimps/bonobos,  even parsimony, unreliable as it is, would suggest that the common ancestor was pretty much Australopithecus-like.
We can extend this argument to orangutans: given the many apparent similarities shared by humans and orangutans but not by chimps or gorillas, these may well have been inherited from an Australopithecus-like ancestor. In this case the arboreal (brachiating) adaptations of all three lineages would have been evolved independently, with different suites of ancestral features retained to be shared with humans.
Personally, I find Filler's hypothesis very convincing, more so than either the Knuckle-walking or the arboreal bipedalism explanations. And this paper provides strong support (although it doesn't say anything against arboreal bipedalism).
Kivell, T., & Schmitt, D. (2009). Independent evolution of knuckle-walking in African apes shows that humans did not evolve from a knuckle-walking ancestor Proceedings of the National Academy of Sciences DOI: 10.1073/pnas.0901280106
Appendix: You can use the back key to return to where you were, or click on the quoted text to return to the line with the footnote.
A1. "Mammals the size of Proconsul spend a lot more energy in vertical movement than horizontal": This is because the mammalian ratio of basal metabolic rate to weight decreases with weight differently than the energy involved in vertical movement varies with weight, as does the energy involved in movement at all. I have been unable to find any discussion of this online, and can't even recall where I read it. I find it hard to believe that this subject has been ignored in discussions of arborial vs. terrestrial movement: I suspect there's something wrong with my search technique.
Basically, an animal the size of a squirrel spends almost as much energy moving horizontally as vertically, and the difference isn't all that large (for mammals with their high metabolic rate) from standing still. Both differences increase with increasing body weight (technically, mass). Obviously, the effect also varies by type of movement.
Links: I've included only the links called out in this leader. Not all of these links are called out in the text. Use the back key if you came via clicking a footnote.
1. Bipedal Humans Came Down From The Trees, Not Up From The Ground ScienceDaily (Aug. 11, 2009) not peer reviewed
2. Independent evolution of knuckle-walking in African apes shows that humans did not evolve from a knuckle-walking ancestor paywall
3. The Upright Ape: A New Origin of the Species by Aaron G. Filler MD, PhD
4. Homeotic Evolution in the Mammalia: Diversification of Therian Axial Seriation and the Morphogenetic Basis of Human Origins open access
5. Locomotion and posture from the common hominoid ancestor to fully modern hominins, with special reference to the last common panin/hominin ancestor paywall
6. Orangutan positional behavior and the nature of arboreal locomotion in Hominoidea
7. Origin of human bipedalism as an adaptation for locomotion on flexible branches free registration required
8. The Origins of Human Bipedalism paywall
9. Comment on "Origin of Human Bipedalism As an Adaptation for Locomotion on Flexible Branches" Open Access
10. Response to Comment on "Origin of Human Bipedalism As an Adaptation for Locomotion on Flexible Branches" Open Access
11. Locomotor Ecology of Wild Orangutans (Pongo pygmaeus abelii) in the Gunung Leuser Ecosystem, Sumatra, Indonesia: A Multivariate Analysis Using Log-Linear Modelling paywall
12. Orangutan Positional Behavior and the Nature of Arboreal Locomotion in Hominoidea
13. The environmental context of human evolutionary history in Eurasia and Africa Open Access