Orrorin

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.

Today I lectured on the earliest hominid samples for my graduate course on australopithecines. This is the first time I have been able to give a full lecture on the Late Miocene hominids up to A. anamensis since their discovery. The thing that struck me is that even if you study a set of fossils and literature for research, there are things that don't really strike you until you are standing in front of a full-screen slide projection talking about them.

One of the interesting things was to see the juxtaposition of the Lothagam and Tabarin mandibles with the new Ardipithecus and other early hominid samples. It's worthwhile remembering that not that long a time ago, Lothagam was the earliest hominid, and was argued to fit within the range of variation of A. afarensis (Hill et al. 1992). Tabarin, likewise, was not specially distinguishable from the A. afarensis sample (Ward and Hill 1987). They undoubtedly remain so, but chronologically they make sense as part of the Ardipithecus sample, which raises the anatomical question: are they Ardipithecus or something very like it? The answers are out there, I set the graduate students on the problem, and I have every confidence they will come up with an answer in the next couple of weeks.

Another observation is the very distinctive mandibular anatomy of A. anamensis The well-preserved mandibles all have very long postcanine tooth rows, certainly compared to the relatively narrow breadth of the dentition. Moreover, the mandibular symphysis is very long and slopes posteriorly to a greater extent than in later hominids (all this reviewed in Ward et al. 2001). This has a couple of interesting consequences. The first is that the mandible begins curving medially toward the symphysis relatively distally--around the first molars. This is exactly the morphology that was said to be hominid-like about Ramapithecus, and indeed the curvature itself is similar to later hominids. What is different about A. anamensis is the extent of the anterior dentition. This all tends to say that A. afarensis was substantially more orthognathic than earlier A. anamensis. A question is whether the other early hominids were similar to A. anamensis in this respect.

As yet, none of the earlier hominid mandibles are sufficiently preserved to evaluate the symphyseal morphology or the shape of the anterior dentition. The maxilla of Sahelanthropus is sufficiently preserved in the Toumai specimen, but it badly needs reconstruction to say for sure what its shape is (Brunet et al. 2002). From the basal view, it appears more apelike in shape than in A. afarensis, but the lower maxilla appears rather less prognathic than in AL 444-2 or other A. afarensis remains, raising doubt as to whether the front of the face was really more projecting than in later hominids.

The question left to answer with these missing observations is whether A. anamensis was intermediate between the earliest hominids and A. africanus in toothrow shape and its anterior dentition, or whether it diverges from both these samples. Its configuration appears unique at the moment, and seems to provide a distinctive combination of posterior tooth expansion, mandibular strengthening and buttressing, and the retention of a large anterior dentition.

How much of a dental difference is there between A. anamensis and Ardipithecus? I ask this because one of the most distinctive differences between A. afarensis and Ardipithecus is the dm₁, which is very apelike in the Aramis ARA-VP-1/129 mandibular fragment (White et al. 1994). The apelike morphology is a mesiodistally long tooth, without buccolingual expansion, and without the elaboration of occlusal topology such as a marked talonid basin. Early hominids have expanded deciduous molars, and the dm₁ in particular is quite molariform (as in the Taung mandible). But the morphology in A. anamensis is close to that described for Ardipithecus. The tooth is best preserved in the KNM-KP 34725 dentition (and is less well preserved but consistent with this form in KNM-KP 31712). The tooth is much longer mesiodistally than buccolingually, and it is narrower than any in the A. afarensis sample (Ward et al. 2001). The only notable difference between this tooth and the Aramis specimen is its larger size, being nearly 2 mm larger in both length and breadth, which makes it more similar in size to an A. afarensis tooth, though not in shape.

What is lacking now is an appreciation of the probable level of variation among the dentitions within a single sample. Here, we face the problem of comparing multiple samples separated by hundreds of thousands of years, without even the possibility of a test of significance between them. For example, the mandibular premolars of A. anamensis are described by Ward and colleagues (2001) as being similar to Ardipithecus in having a unicuspid P₃ and a less expanded talonid on the P₄ compared to A. afarensis. But the P₃ form is highly variable at the single site of Hadar, as the form of the upper canine shows substantial variation in only a few specimens at Laetoli and Hadar. If the earlier hominids are all fairly similar, is this to be interpreted as an important degree of similarity compared to later hominids? Is there any substantial evidence of multiple species here at all? Tough question (Ward et al. 2001 duck it by noting that descriptions of Ardipithecus and Orrorin are lacking).

It is probably necessary to look into the quantification of nonmetric variation within dental samples of early hominids. This will be tough since there are really not enough teeth to create good seriations to examine character variation. But the diagnosis of A. kadabba (Haile-Selassie 2001) is an interesting case study in the delineation of minor morphological details. In this instance, only one specimen of each potential subspecies (now species, and one specimen published, although surely the author saw a broader sample of unpublished remains) were compared with each other. Each difference was tabulated as part of the subspecies diagnosis (without direct consideration of whether the traits might vary in earlier or later species or samples). How likely is it that two fossils within a sample will differ in the presence of a shallow mesial fovea on P3? Or in the diagnosis of the species (Haile-Selassie et al. 2004), how likely is it that two specimens will differ as A. kadabba and O. tugenensis evidently do by a more circular canine shape in occlusal view? This is the important kind of question for testing the validity of the diagnosis, but it is as yet unanswered.

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 418:145-151.

Haile-Selassie Y. 2001. Late Miocene hominids from the Middle Awash, Ethiopia. Nature 412:178-181.

Haile-Selassie Y, Suwa G, White TD. 2004. Late Miocene teeth from Middle Awash, Ethiopia, and early hominid dental evolution. Science 303:1503-1505.

Hill AH, Ward S, Brown B. 1992. Anatomy and age of the Lothagam mandible. J Hum Evol 22:439-451.

Leakey MG, Feibel CS, MacDougall I, Walker A. 1995. New four-million-year-old hominid species from Kanapoi and Allia Bay, Kenya. Nature 376:565-571.

Semaw S, Simpson SW, Quade J, Renne PR, Butler RF, McIntosh WC, Levin N, Dominguez-Rodrigo M, Rogers MJ. 2005. Early Pliocene hominids from Gona, Ethiopia. Nature 433:301-305.
Review on this site

Senut B, Pickford M, Gommery D, Mein P, Cheboi K, Coppens Y. 2001. First hominid from the Miocene (Lukeino formation, Kenya). C R Acad Sci Paris Sciences de la Terre et des planetes 332:137-144.

Ward CV, Leakey MG, Walker A. 2001. Morphology of Australopithecus anamensis from Kanapoi and Allia Bay, Kenya. J Hum Evol 41:255-368.

Ward SC, Hill A. 1987. Pliocene hominid partial mandible from Tabarin, Baringo, Kenya. Am J Phys Anthropol 72:21-33. PubMed

White T, Suwa G, Asfaw B. 1994. Australopithecus ramidus, a new species of early hominid from Aramis, Ethiopia. Nature 371:306-312.

WoldeGabriel G, White TD, Suwa G, Renne P, deHeinzelin J, Hart WK, Helken G. 1994. Ecological and temporal placement of early Pliocene hominids at Aramis, Ethiopia. Nature 371:330-333.

News story at MSNBC

News story at BBC

Paleoanthropologist Sileshi Semaw has a new paper in Nature describing fossils of Ardipithecus from the Gona research area in Ethiopia. Semaw is a researcher at the CRAFT Stone Age Institute at the University of Indiana. (I would just like to enter a note here that the web pages of the CRAFT Institute and the Department of Anthropology at Indiana are extraordinarily difficult to find and use. Can you imagine a university department with a Flash-only website? Compared to this, the CRAFT page is easy to use, but hard to find. The most important problem is that the word "CRAFT" appears nowhere on the site or its address (www.stoneageinstitute.org), and so searches don't find it! Maybe it will move up the Google rankings soon....)

The fossils come from a locality called As Duma, and likely date to between 4.3 and 4.5 million years ago, based on stratigraphic and paleomagnetic considerations. The remains are mostly dental, with three substantially preserved dentitions and several isolcated teeth. There is also a fragment of mandibular corpus and a mandibular ramus matched with one of the mandibular series. Otherwise, there are three hand bones (phalanges) and one toe bone.

Is there evidence for bipedality?

As is the case for other remains from Ardipithecus, here it is argued that the toe bone represents a biped, because the proximal articular facet is oriented upward (dorsally). This means that the toes were characteristically dorsiflexed rather than plantarflexed, and therefore were used for walking but not substantially for gripping objects.

Why are the fossils assigned to Ardipithecus?

The teeth resemble known dental remains of Ardipithecus. General similarities include the size of the postcanine teeth, the height of the upper and lower canines, and the diamond-like shape of the upper canine in labial view (the broadest mesiodistal point is about halfway between the apex and base of the crown). These features are not entirely compelling because of the notable variability among early australopithecines, including A. anamensis and A. afarensis. According to Semaw and colleagues,

The P₄ crown is mesiodistally compressed with an oval plan, a simple cusp pattern and a single root matching the Aramis (Ethiopia) specimens of Ardipithecus ramidus and distinct from the triangular/quadrangular cervical cross-section of Australopithecus multi-rooted P₄.

In other words, the fossils "fit" well with Ardipithecus by virtue of their anatomy and date, and have at least one tooth crown that is fairly distinctive.

Is there any other Ardipithecus insight?

The evolving story of Ardipithecus is that it is a likely ancestor of later hominids. Contrast this with the situation in 1995, shortly after the initial announcement of both Ardipithecus ramidus and Australopithecus anamensis. These two hominid species overlapped in time, but had clear anatomical differences. Although Ardipithecus had an earlier range of dates (4.1 million to 4.4 million years ago according to White et al. 1994), it was viewed to be morphologically distinct from all later hominids, in particular having molars that were described as smaller, with thinner enamel and more chimpanzee-like morphology than any known australopithecine.

But being described as "chimpanzee-like" has obfuscated much about the anatomy of Ardipithecus. Consider the dental features of A. afarensis compared to living apes and humans: it has thick molar enamel, large molars, molars that increase in size posteriorly, canines that are variable in height, ranging on the small end to incisor-sized, and on the large end still much shorter than females of living ape species. Australopithecines evolved from apes with large projecting canines. It is unclear whether the Miocene apes that were ancestral to later hominids had thick or thin enamel, or large or small molars, because these traits are variable among Miocene hominoids. But they certainly had smaller molars and premolars than the australopithecines, and could not have matched their enamel thickness. Therefore, it is exceedingly likely that the early ancestors of the australopithecines had smaller molar sizes, thinner molar enamel, larger canines, and cutting P₃'s. Compared to A. afarensis these ancestors would be chimpanzee-like in these details.

Is this what the initial description of the Aramis hominids described? Let's consider what White and colleagues (1994) wrote:

Morphology of the known Aramis canines, however, diverges from that of known apes. The upper canines are slightly less incisiform than homologues of A. afarensis but more incisiform than any ape counter part, with occlusally placed terminations of the mesial and distal apical crests. The visual result of apically placed crown shoulders is a low, blunt canine tooth relative to more projecting ape canines, a morphological condition which may have important evolutionary implications. The Aramis upper canine is large buccolingually, formaing a further contrast with mesiodistally elongate African ape canines. Wear pattern also differs significantly from the ape condition. Mandibular canine wear does not show the pattern typical of great apes. (p. 308)

The broken canines and lower P₃ in ARA-VP-1/128 and -6/1 exhibit thin enamel distinct from previously known hominid conditions. Canine enamel thickness approximates the chimpanzee condition, with a lack of apical thickening we observe in other hominids. ... The relatively thin enamel and large size of the Aramis canine, together with its primitive P₃ morphology, suggest a C/P₃ complex morphologically and functionally only slightly removed from the presumed ancestral ape condition. (p. 308)

The ARA-VP-6/1 P₃ is markedly more apelike than any A. afarensis homologue in its high protoconid with extensive buccal face and steep, distolingually directed transverse crest. In these features it is indistinguishable from ape homologues. (p. 308)

Molar morphology resembles the A. afarensis condition, but lacks the extreme buccolingual breadth relative to mesiodistal length common in that species. The 'serrate' root pattern and deep dentine wear on the buccal cusps described in A. afarensis, Tabarin, and Lothagam also occur in Aramis specimens. All molars lack the extensive crenulation and broad occlusal foveae characteristic of modern chimpanzees, or the high cusp topography of gorillas. (p. 309)

On these dental characters, the Aramis hominids do correspond to what we might expect of an ancestor of later hominids. The "chimpanzee-like" character is canine enamel thickness. Other characters are either near or within the range of later hominids, or more apelike. In this context, apelike means that these characters are not specifically similar to any living ape, and indeed the living apes are substantially different from the Aramis remains in several characters. In particular, the chimpanzee-like dm₁ is not specifically like chimpanzees, but instead is in the range of all living and fossil apes. This is a plesiomorphy, not a derived similarity with chimpanzees.

Aramis enamel thickness is similar to chimpanzees not only in the canines but also in the molars. But enamel thickness itself is a problematic character. White and colleagues (1994) say:

A distinct difference from known hominids occurs in molar enamel thickness. Maximum radial enamel thickness of crown faces can be measured in three fractured Aramis specimens and it ranges from 1.1 to 1.2 mm buccally, at or near the unworn cusp apex, perpendicular to the enamel-dentine junction. These values are comparable to the uppermost range of our homologous enamel thickness values measured on broken P. troglodytes molars (n=22; M₁ through to M₃). Equivalent measures in A. afarensis range from 1.4 to 2.0 mm (n=5). (p. 309)

Of course, this places the Aramis specimens intermediate between chimpanzees and other early hominids. White and colleagues (1994) did not report the range of the chimpanzee comparative sample, so it is hard to say what the import of the enamel thickness of Aramis really is. Haile-Selassie (2001, 180) writes:

Another candidate for hominid ancestry is the recently described Orrorin tugenensis. The authors report thick molar enamel and suggest that Ardipithecus and African apes are commonly derived in having 'thin' enamel. However, enamel thickness is a complex character and intraspecifically variable, and its within-tooth three-dimensional patterning is characteristically expressed both serially and taxonomically. Therefore the simplistic dichotomous characterization of enamel as either 'thick' or 'thin' on the basis of unspecified measurements of naturally broken sections (as was done in the Orrorin report) is problematic.

Of course we can compare this quote with the report of Senut and colleagues (2001, p. 4), "Enamel thickness at the apex on the paraconid [of the BAR 1000'00 left M₂] is 3.1 mm. This is comparable to other hominids, Ardipithecus excluded." There certainly does seem to be a difference between the Middle Awash sample and Lukeino in enamel thickness, based on the limited number of examples. It is a shame that the range of variation in living hominoids has not been better reported in the context of these early hominids. But even if everything rises or falls based on enamel thickness alone, we have one sample (Middle Awash) with an intermediate morphology between australopithecines and chimpanzees, and another sample (Lukeino) with an australopithecine-like morphology, which is probably also more similar to earlier Miocene apes like Ouranopithecus.

White and colleagues have clearly moved toward an interpretation of the early hominids in which the taxonomic diversity was minimal. For example, Haile-Selassie, Suwa and White (2004, p. 1505) wrote:

Metric and morphological variation within available small samples of late Miocene teeth attributed to A. kadabba, O. tugenensis, and S. tchadensis is no greater in degree than that seen within extant ape genera. Despite claims of molar enamel thickness differences among these late Miocene fossils, we question the interpretation that these taxa represent three separate genera or even lineages. Given the limited data currently available, it is possible that all of these remains represent specific or subspecific variation within a single genus.

One may point out that if the Asa Koma and Lukeino hominids actually do represent a single species, they are properly referred to Orrorin (or Ardipithecus) tugenensis, rather than A. kadabba. One may speculate that it is for this reason that Haile-Selassie, Suwa and White (2004) focus on the genus level in their argument, since it is at this level that Ardipithecus has priority. It is worth mentioning that the enamel thickness in the A. anamensis molars is more similar to later australopithecines than to Ardipithecus, with measurements around 1.9 mm on the protocone of KNM-ER 30748 (Ward et al. 2001). Again, the measurements here emphasize the problems with comparison of such values, since measurements on fossils are taken where breaks naturally occur, and with the possibility of attrition on the teeth.

At any rate, this argument continues with the discovery of the Gona Ardipithecus remains. According to the BBC, Tim White

agreed it was becoming apparent A. ramidus was an important species that was a very plausible ancestor to later hominids. "It's already clear that we're seeing the basic grade from which Australopithecus evolved,"he told the BBC News website.

One feature of these hominids points toward that conclusion--even at the expense of A. anamensis. The reconstruction of the GWM-3/P1 mandible has a shape similar to AL 288-1 (Lucy) with diverging (V-shaped) tooth rows. Semaw and colleagues contrast this morphology with A. anamensis, where the tooth rows are oriented parallel to each other.

Is it possible that the Kanapoi and Allia Bay hominids were a side-branch of an Ardipithecus--A. afarensis lineage? Sure, there is actually little to preclude this scenario beyond the relatively thicker enamel and larger molars of the sample assigned to A. anamensis. It would be helpful to have a full characterization of the variability of these samples as they existed over time, to judge the magnitude of change necessary under different evolutionary scenarios.

But there is one more point on which White and colleagues (1994) described Aramis as chimpanzee-like: the basicranium.

The ARA-VP-1/125 and -1/500 specimens represent adult temporal and occipital regions. Both are smaller than their A. afarensis counterparts, but no female temporal is known for that species. The Aramis cranial fossils evince a strikingly chimpanzee-like morphology that includes marked pneumatization of the temporal squama which even invades the root of the zygoma. (p. 310)

And the postcranial remains are described as displaying "a mosaic of characters usually attributed to hominids and/or great apes" (p. 311). In fact, the known postcrania are an area of resemblance between Ardipithecus and A. anamensis, since both these samples appear to have relatively long forelimb bones compared to later hominids (this comparison is imperfect since body size is not known from other evidence). And the basicranium of A. anamensis was probably similar to Aramis, considering that the KNM-KP 29281 temporal appears to have been pneumatized in the same areas as its Aramis counterpart where it is preserved (Ward et al. 2001). Much appears to have been similar between these two samples, just as much is similar among the earlier hominid samples.

Is this a single lineage changing over time? That would be an appropriate null hypothesis to pursue, and there is little evidence tending to refute it now.

References

Semaw S, Simpson SW, Quade J, Renne PR, Butler RF, McIntosh WC, Levin N, Dominguez-Rodrigo M, Rogers MJ. 2005. Early Pliocene hominids from Gona, Ethiopia. Nature 433:301-305. Full text at Nature

The earliest skeletal traces of bipedalism come from the fossils from Lukeino, in the Tugen Hills of western Kenya. A single isolated molar was found here in 1975 by Martin Pickford. Renewed surveys beginning in 2000 recovered additional specimens, including three proximal femora, a distal humerus with shaft, and most of a mandible. The deposits date to approximately 6 million years ago (Senut et al., 2001).

Human and chimpanzee femora are mostly similar on their proximal ends. They both have femur necks of about the same relative length, and both have angles between the neck and the shaft of between 110 and 130 degrees (Aiello and Dean 1990). This means that fossil remains of proximal femora are not the most obvious indicators of bipedal locomotion.

But a few telling differences divide the two species. The most functionally significant difference is the distribution of cortical bone in the femur neck. The long bones have dense layers, called cortical bone, that make up the shaft and the surfaces of the proximal and distal ends. Much of the proximal and distal ends of the bones are, however, made up of thin plates of bone arranged in a spongy texture, called trabecular bone. The distribution of cortical bone compared to trabecular bone in the femur neck reflects the way that force was habitually applied to the bone during life. In a biped, the cortical bone is thicker at the bottom of the femur neck than at the topÑbecause while the mass of the body applies bending force to both the top and bottom of the femur neck, the bending at the top is reduced by the pull of large muscles that support the body. In non-bipeds like chimpanzees, the cortical bone is equally thick on both the top and bottom of the femur neck (Lovejoy 1988). The difference between these thicknesses on the Lukeino femora shows they were bipedal, similar to those of later known hominid fossils (Galik et al. 2004).

More on Lukeino

More on bipedalism

Compared to their small body mass, the forelimbs of early hominids are both longer and more muscular than those of recent humans. The arms are shorter than in chimpanzees, but the areas of muscle attachment have greater strength. Strength is especially evident in a large humerus from the Ethiopian site of Maka, dating to 3.4 million years ago (White et al. 1993). The prominent muscle attachments on this large specimen indicate that the individual was very strong, but also that most muscle exertion was in a single preferred pattern. The bone is thicker than chimpanzee humeri of equal length, again reflecting its mechanical strength.

Several other forelimb fossils show a similar pattern. These include a relatively large distal humerus fragment from Kanapoi, a large radius from the contemporary site of Sibilot Hill, and a distal section of humerus exhibiting large muscular crests from Lukeino (Senut et al. 2001). Additionally, the hamate bone preserved at the Kenyan site of Turkwel preserves part of a very large carpal tunnel region, indicating strong tendon attachments into the hand (Ward 1999). Finally, the finger bones of early hominids are curved. This feature occurs wherever Early Pliocene hominid finger bones are preserved (Stern and Susman 1983).

The most probable interpretation for the strength of the forelimbs among these sites is that early hominids were effective climbers. Hominids do not have grasping feet. Apes use all four limbs in a variety of climbing positions, but hominids use their arms mainly to pull the body upward with the legs providing upward propulsion but no gripping support. Such use would lead to large muscle development in the arms, both because they bore more of the force of climbing and because they functioned in a more specialized way.

But despite the strength of the large fossil arms, smaller individuals show a somewhat different pattern. For example, the AL 288-1 skeleton preserves much of both humeri and ulnae, and these small bones bear minimal muscle markings. The difference in forelimb anatomy between large and small individuals may mean either that males climbed more frequently than females or that the biomechanics of climbing among malesÑwith a mass much larger than femalesÑplaced much greater muscle requirements on the male forearm.

Males may have performed other tasks with their arms, including wielding weapons or other competitive behaviors such as threat displays. The hands of early hominids, as represented at Hadar, have fingers that are similar to living humans in their relative sizes. These proportions are very different than in chimpanzees, which have a much shorter thumb that departs the hand much closer to the wrist, as well as much longer fingers. The human-like proportions of the hands underline the fact that climbing in these obligate bipeds was done in a human-like manner, and their hands did not function in a chimpanzee-like suspensory role. Also, early hominids may have gripped clubs or other items that do not require forceful fingertip control. Chimpanzees wield large branches in the context of threat displays, and it is possible that early hominids also had such behaviors or even more menacing ones, enabled by the power of arms like those from Maka.

However, early hominid hands were clearly not used for making stone tools. Two sources of evidence argue against the ability of these early hominids to modify stone. First, no stone tools have yet been found earlier than about 2.6 million years ago, long after the early Hadar sample. Second, the Hadar hands and other early hominid hand bones lack important features that reflect a powerful grip useful for tool production (Marzke 1983). Most noticeably, the distal finger bones, or phalanges, lack the large fingertip surfaces, called apical tufts, which are found in living and fossil humans (Bush et al. 1982). These large fingertips increase the surface area used for gripping, and allow the forceful grip necessary for tool production. The apical tufts at Hadar are relatively much smaller than those in human fingers (Stern and Susman 1983).