Pliocene

UPDATE (2011-09-06) Note: The conclusions of the research were later critiqued, I posted on that criticism after this post.

Shannon McPherron, Zeresenay Alemseged and colleagues working at the Dikika field site in Ethiopia have found evidence of stone tool use 3.39 million years ago [1]. That's 800,000 years earlier than the previous first-known tool use, and occurs during the existence of Australopithecus afarensis.

The evidence is a series of cutmarks and one percussion mark on two bovid bones. One is a piece of rib from a large "cow-sized" animal, the other a femur fragment from a smaller "goat-sized" bovid. The analysis goes through several microscopic comparisons to rule out alternative causes for the cutmarks, such as trampling. The key paragraph of the results:

The cut marks demonstrate hominin use of sharp-edged stone to remove flesh from the femur and rib. The location and density of the marks on the femur indicate that flesh was rather widely spread on the surface, although it is possible that there could have been isolated patches of flesh. The percussion marks on the femur demonstrate hominin use of a blunt stone to strike the bone, probably to gain access to the marrow. The external surfaces of ribs have thin sheaths of flesh, so the scraping marks on the fossil rib suggest stripping off of these sheaths.

I have some lingering doubts, none of which are very serious, but that point out the need to look harder at other sites. It sure would have been nice if they'd found an anomalous sharp-edged rock nearby.

The two bones are compelling, but the study does not give much indication of how representative they are. How many similar-sized bone fragments were left at the site? How many were collected? What fraction of "cutmarked" bones does that make? What fraction show signs of trampling and various kinds of post-depositional damage?

Those questions are essential to answer the "green car" problem. If you don't know this one, it's fairly simple -- a witness reports a green car leaving the scene, and green cars are very rare -- the police think this is a great lead. But blue cars are very common in the city, and there is a small chance that the witness mistook a blue one for a green one. Whether it actually was a green car depends on the actual proportion of green to blue cars, and the actual probability that the witness was wrong.

In this case, I think there is a very small chance that the marks on these bones could have been produced by processes other than deliberate cutting by a stone tool. But in a sample of hundreds or thousands of bone fragments, a small chance might well happen a couple of times. It's very difficult to quantify this, because archaeologists don't collect every bone fragment. The only real way to address the problem is to find more cutmarks and do other statistics on them -- do they occur where flesh is attached to bone, etc.

It does seem odd that nobody's identified clear stone tools, which are in later sites a lot more common than cutmarked bones. A tool-user will make many artifacts during her life. (Why "her"? Well, in chimpanzees, it's the females who dominate technology transmission...) We have a lot of australopithecine bones. If this was a long-lasting tradition, we should have found a lot of stone tools by now.

Maybe it wasn't a long-lasting tradition. Chimpanzee technology is significantly clustered geographically, some of the most interesting behaviors have been observed only at a single field site. If Australopithecus had a similar pattern of cultural diversity, tool use may have been innovated many times without "catching on" over a wide geographic or temporal extent. Here's what McPherron and colleagues conclude along similar lines:

Whether A. afarensis also produced stone tools remains to be demonstrated, but the DIK-55 finds may fit with the view that stone tool production pre-dates the earliest known archaeological sites and was initially of low intensity (one-to-a-few flakes removed per nodule) and distributed in extremely low density scatters across the landscape such that its archaeological visibility is quite low (16).

Or maybe we just haven't noticed. Fluvial contexts may have been bad places for Australopithecus to hang out. McPherron and colleagues allude to this explanation for the local absence of tools at Dikika:

However, stone tool production and consequently archaeological accumulations are not expected at this locality given the sedimentary environment characterized by the palaeo-Awash River emptying into a nearby lake (3, 4). In this relatively low-energy depositional environment, clasts suitable for stone tool production are not present (few particles larger than fine gravel, 8 mm diameter). Within the exposed SH Member, the distance from DIK-55 to cobble-sized raw materials (>64 mm) is ~6 km (at Gorgore; Fig. 1). Thus, in this instance the absence of evidence for stone tool production in the immediate vicinity of the cut-marked bones may reflect landscape-level raw material constraints.

The research article is accompanied by an essay by David Braun reviewing the find [2]. He stretches a bit, but I think the interpretations he suggests are worth airing. One -- why are there cutmarked bones 6 km from any good source of stone raw material?

The meat and marrow of large animals must have been a valued resource, because McPherron et al. conclude that the tool users incurred the cost of transporting stones 6 kilometres from where they occurred naturally to the site where the butchery took place. Further costs that were associated with the consumption of carrion, and were apparently worth the risk, include exposure to parasites and competition with large carnivores.

Two -- what about the "meat-brain" connection?

This provides exciting evidence of how A. afarensis behaved. At one time, the species was considered to be a relatively primitive hominin, but this perception is being redefined. For example, it now seems that Lucy's kin had body proportions that were more similar to those of humans than of apes (6). Analyses of the hand of A. afarensis show that it had relatively short fingers that would allow the kind of fine-scale manipulation necessary for tool use (7). A recently discovered skeleton from the Woranso–Mille area of Ethiopia suggests that A. afarensis did not have the ape-like, 'funnel-shaped' thorax usually associated with a large digestive tract and low-quality diet (8). Perhaps the findings that these hominins used tools and had a carnivorous component to their diet should not have been so unexpected.

A 2.6-million-year-old butchery tradition should already have refuted the hypothesis that meat-eating caused the expansion of brain size in Homo. But it was still possible to maintain that the initial Oldowan was insufficiently dedicated, or that the anatomical specializations (e.g., small guts) allowing brain expansion took time to develop, or that as-yet-undiscovered large-brained hominins would be found. Any of these are still possible, but the observations Braun points out pretty much demolish the 15-year-old story of "expensive tissue." Australopithecus seems to have had a small gut, and a bigger brain than chimpanzees. If there was a tradeoff, A. afarensis had already made it.

Braun didn't mention A. sediba, which adds another wrinkle. A late species of Australopithecus with human-sized teeth. Or (as some prefer), a pre-habilis species of Homo with an Australopithecus-sized brain. What was its diet like? I have a feeling we'll know before too long.

Meanwhile, I'll be floating for the rest of the year, since I included this as the far-out "bonus" entry in my 2010 New Year predictions! You know, the one that's so bizarre that it seems like it'll never happen. Heh.

UPDATE (2010-08-11): John Noble Wilford got ahold of some skeptics for his NY Times story on the discovery:

Still, the discoverers are already being pressed to defend their interpretation that the cut marks on the bones are evidence of stone-tool butchery. Tim D. White of the University of California, Berkeley, one of the foremost investigators of early human origins, said flatly that their “claims greatly outstrip the evidence,” and noted, “We have been working sites in this area for 40 years, and not a single stone tool has been found in deposits of this antiquity.”

Sileshi Semaw, a paleoanthropologist at Indiana University who was a discoverer of the oldest confirmed stone tools, from 2.6 million years ago, noted in an e-mail message from Ethiopia that researchers had often been misled by bone markings left by trampling animals and other natural causes. “I am not convinced of the new discovery,” he said.

UPDATE (2010-08-12): Maybe some are looking for more about australopithecine diets. My post from 2005, "Chemistry and early hominid diets" has a good compilation of stable isotope observations and what may explain them. With the cutmark evidence, you can read through the discussion of C₄ plant contributions, and think about the grazers that A. africanus may have been eating.

UPDATE (2010-08-16): Science Friday with Ira Flatow covered this story last week, including commentary by Alemseged and David DeGusta, who suggests that the marks may be crocodile bite marks. Doesn't look like it to me, but as I wrote above, I'd like to see statistics on a few hundred damaged bones to see the probability that an arbitrary one will look like stone cutmarks.

References

The other day, I started writing about the Sarmiento-White exchange on Ardipithecus, by describing how they disagree about the implications of the molecular clock.

What really prompted me to break up my discussion into three posts was that it takes quite a lot of space to explicate the features of the pelvis. I've taken care to reference the description by Lovejoy and colleagues (2009c), the general discussion of Ardi's locomotor anatomy in Lovejoy et al. (2009a, 2009b), and the discussion of early hominin pelvic evolution by Lovejoy and colleagues (1999).

I have a major hesitation that keeps me from writing anything about the Ardipithecus pelvis beyond those descriptions: Independent investigators at present cannot verify or replicate any comparisons made in Lovejoy and colleagues' analyses. Most of the measurements and many quantitative observations depend on a 3-d model. That model is not available for inspection, and the published description does not provide enough detail about the model to independently assess its accuracy. Worse, as I discussed last fall, the model appears to have been derived from the a priori expectations about pelvis evolution that Lovejoy and colleagues published in 1999.

As a result, I don't think any independent reader, including me, can tell how much of the model is real.

Given my problems understanding their pelvis 3-d model, I've decided to limit myself to the narrow points considered by Sarmiento's (2010) comment and White and colleagues' (2010) reply. Lovejoy and colleagues (2009b, 2009c) claimed that most of the pelvic anatomy of Ardipithecus is primitive for great apes, and that many of the pelvic features shared by chimpanzees and gorillas evolved in parallel in those two lineages. But they listed a few features that they considered to be derived in Ardipithecus and shared with Australopithecus. Sarmiento lists these, together with two features of the foot, and argues that they are not compelling evidence that Ardipithecus is a cladistic hominin:

Of the remaining characters listed as common to Ardipithecus and Australopithecus, none of the eight postcranial characters (sagittal iliac/isthmus orientation, slightly broadened iliac breadth, strong anterior inferior iliac spine formed by separate ossification center, robust second metatarsal base and shaft, dorsally domed second to fifth metatarsal heads, upwardly canted proximal foot phalanges, and short iliac isthmus and pubic symphysis outline), nor the other four craniodental characters [anterior basion position (14), advanced cranial flexion, and broad lower molars and mandibular corpus] are shown by systematic comparisons to be exclusive to humans or share-derived with humans. Nearly all are quantitative characters that appear in early hominoids (i.e., Oreopithecus and Dryopithecus) and have appeared independently in other primate lineages, and character simplicity is such that parallelisms or reversals in polarity cannot be demonstrated (12, 15).

I think Sarmiento's argument is entirely reasonable. Lovejoy and colleagues (2009a, 2009b) claimed a long series of parallelisms between chimpanzees and gorillas. Despite some reservations, I tend to agree -- Ardipithecus is primitive in its postcranial anatomy, and living apes are convergently derived. But take the argument to its logical end, and it becomes Sarmiento's. Ardi shares some postcranial features with hominins that living apes lack, but how do we know that any of them are derived? Or if they are derived, how do we know that they aren't trivially simple to evolve in parallel?

In their published reply to Sarmento, White and colleagues do not mention the long series of great ape postcranial features that they previously argued to be cases of parallel evolution (Lovejoy et al. 2009b, 2009c). Instead, they claim that three features of the pelvis are so convincingly like Australopithecus that Ardi must be a hominin:

Although isolated aspects of pelvic morphology of Oreopithecus may partially mimic those of Ar. ramidus [such as a projecting anterior inferior iliac spine (AIIS)], crucial postcranial elements of the latter (9, 10) are unambiguously derived toward the Australopithecus condition, to the exclusion of Oreopithecus. Some of these derivations probably stem from shared changes in pattern formation exhibited by both Ar. ramidus and Australopithecus. In the pelvis, these include (i) superoinferior approximation of the sacroiliac and acetabular joints by iliac isthmus shortening and (ii) a sagittally oriented and greatly broadened lower iliac isthmus accompanied by (iii) an exaggerated anterior margin, itself the product of a unique physis for the AIIS, shared only with phyletic hominids.

I find this reply very strange. The "shared changes in pattern formation" hypothesis actually supports Sarmiento's argument. If White and colleagues are correct about the morphogenetic basis of the Ardipithecus pelvic anatomy, that makes it more likely to have evolved convergently with Australopithecus, not less likely. Lovejoy and colleagues (1999) emphasized this point -- the pelvic features of hominins were likely to have evolved due to selection for a shorter pelvis, principally for biomechanical reasons, with other characters of the pelvis and femur changing entirely due to their genetic correlation with this major target of selection.

The reply omits the most persuasive of the derived features in hominins -- the short ilium -- which was at the center of Lovejoy and colleagues' (1999) account of hominin pelvic evolution. Here's a comparison of 3-d models:

Ardi looks very obviously like the human and Lucy, and very different from the chimpanzee, right? But I think that the chimpanzee model in this picture is larger than it should be, as the acetabulum looks much larger than Ardi even though Lovejoy and colleagues (2009c) report Ardi's acetabulum as right in the middle of the chimpanzee range. Maybe they chose a large chimpanzee, or built the Ardi 3-d model using the smaller end of their range of possible acetabular diameter. You see the problem of using a model instead of the actual fossil?

In any event, the differences between Ardi's os coxa and the chimpanzee's are obvious. Ardi has a much shorter ilium. The chimpanzee has an iliac blade that comes right out of the picture toward us, because it is oriented along a coronal axis. Ardi's angles forward, or anteriorly, like the hominins.

In fact, if we look at the model in superior view superimposed on Lucy's pelvis, you can see that Ardi's iliac blades angle even more anteriorly than Lucy's:

The three features White and colleagues (2010) list, as quoted above, are morphological side effects of the shorter, more sagitally angled ilia. Lovejoy and colleagues (1999) paper would likely have described these features as side effects of selection for a shorter pelvis with an anteriorly directed origin for the rectus femoris muscle.

The question is: How much of the functional similarity between Ardi and hominins is homology, and how much is convergence? Similarity may not reflect homology -- descent of the feature from the same ancestor.

That point is especially notable when White and colleagues (2010) discuss Oreopithecus -- an extinct ape whose pelvis shares some features with hominins, and other features with apes. Oreopithecus is not a hominin, but it may have had some adaptations to a bipedal stance. Yet it also shares features that Lovejoy and colleagues (2009b) have argued must have evolved convergently in orangutans, chimpanzees and gorillas. That seems like a real problem for the idea that Ardipithecus represents the primitive condition for such traits.

Here's the Oreopithecus paragraph from White et al. (2010), the first time that Ardipithecus and Oreopithecus pelvic features have been compared (other than here on the blog):

Indeed, Oreopithecus diverges from hominids remarkably in features ranging from limb proportions to dental anatomy. In the pelvis, it features bi-iliac entrapment of at least one lumbar vertebra and general immobilization of the lumbar column (including transformation of lumbar somites into its six-segment sacrum). Such changes stand in stark contrast to the six lumbar, four-segment sacrum of Au. afarensis, a character adumbrated by the precipitous reduction in iliac height (and extensive broadening) of the Ar. ramidus ilium (10). African apes have entirely rigidified lumbar columns that differ radically from those of hominids.

I think this comparison is very important. Oreopithecus is not a member of the orangutan clade, and Lovejoy and colleagues' (2009b) scenario implies that if Oreopithecus is a member of the African ape clade, it -- like chimpanzees and gorillas -- must have evolved these features convergently.

Can it be that orangutans, chimpanzees, gorillas, and Oreopithecus all acquired the distinctive "bi-iliac entrapment" of the lower lumbar vertebrae in four separate instances of evolutionary convergence? Put those together with the elongation of the arms, reduction in the length of the lumbar column, and sacralization of lumbar vertebrae. Far from a simple change, it a series of complicated, correlated changes. Lovejoy and colleagues (2009b) defended the hypothesis that these traits are parallelisms shared by all the lineages of living great apes. Now, White and colleagues (2010) are forced to posit a fourth independent evolution of many of these traits in Oreopithecus.

Despite those similarities to living great apes, Oreopithecus shares with hominins the development of a relatively prominent anterior inferior iliac spine. This implies an adaptation to hip flexion or knee extension with a more extended leg. Bipedal stance is one possible explanation for this anatomy, and is the explanation that Lovejoy and colleagues (2009c) offer for its presence in Ardipithecus. White and colleagues (2010) include this as their feature (iii), the "unique physis for the AIIS, shared only with phyletic hominids." But this description seems exaggerated, when we consider what Lovejoy and colleagues (2009c:71e3) actually wrote:

The form and size of the AIIS in ARA-VP- 6/500, as well as its projection anterior to the acetabular margin, indicate that this structure had already begun to appear and mature via a novel physis.

A "novel physis" refers to a separate growth plate for the anterior inferior iliac spine. Ardi was an adult, and her pelvis was fully developed. So there's no observing whether the anterior inferior iliac spine had its own growth plate. Lovejoy and colleagues (2009c, 2010) are just claiming there must have been one. What basis could there be for such a model, other than an allometric analysis of the anterior inferior iliac spine in humans and other primates where it is present -- such as Oreopithecus? Remember that Ardi is more than twice the body size of Oreopithecus, yet Rook and colleagues (1999) showed that the cancellous structure within the anterior inferior iliac spine of Oreopithecus is a close match to Homo. That anatomical similarity may imply a common developmental pathway in Oreopithecus and hominins.

Is the anterior inferior iliac spine homologous in Oreopithecus and Ardipithecus? If so, it is probably primitive for great apes, not derived in hominins. Does it have another functional role besides bipedal stance? If so, that functional role might well have occurred in Ardipithecus, another arboreal quadruped.

Could other features of Ardi's pelvis be consequences of arboreal quadrupedal locomotion in an ape with a long lumbar spine? The sagittal orientation of the iliac blades and isthmus is not like living great apes, but it is like living Old World monkeys. Ardi's ilia are shorter than monkey ilia, but the question deserves some serious allometric study. Also deserving of study is whether isthmus orientation in monkeys matches that of the iliac blades, and if not, why not? One hypothesis would be the morphogenetic effects of selection for a shorter ilium length, the scenario published by Lovejoy and colleagues (1999).

I don't think there's any question that the evolutionary scenario outlined by Lovejoy and colleagues (2009b) is highly non-parsimonious with respect to the postcrania. It requires the convergent evolution of a long suite of characters within all the living great apes in at least three separate evolutionary histories. Add in fossil apes -- at least Oreopithecus, and possibly Morotopithecus and Dryopithecus -- and the number of parallelisms is extreme. The chimpanzee-gorilla convergences go even further beyond those shared with orangutans to include the knuckle-walking features of the wrist and hand, and several dental characters.

White and colleagues (2010), as I'll describe in the next post, argue that the shared dental characters of Ardipithecus and Australopithecus necessitate their close relationship. Once this is assumed, the many postcranial convergences become necessary. In that perspective, it helps to "soften the blow" somewhat by identifying those postcranial features shared by Ardipithecus and the hominins.

From the perspective of the pelvis, I'll return to one feature of Ardipithecus that seems independent, shared with hominins, and lacking in Oreopithecus: the "precipitous reduction in iliac height," so obvious in the picture above. But Ardi's os coxa is badly crushed at the superior border of the ilium. My post from last fall includes photos of both Ardi's os coxa and the pelvis of Oreopithecus. Ardi's is relatively shorter, no question, and it lacks the great height on its medial aspect, that creates the "entrapment" of the last lumbar vertebra of Oreopithecus. But the crushing seems to obscure this anatomy, so that it's not possible to be sure from the photos.

I wish we had better than a cartoon model to compare. During the seven months since I first detailed what I see as weak points in the pelvic description, I've become less and less persuaded that the pelvic features reflect any hominin-like locomotor adaptations in Ardipithecus. There are many unresolved functional issues, which obscure the phylogenetic relations between living and fossil apes. Ardi makes every tree less parsimonious, no matter which branch we put her on. Shoe-horning her into the hominins doesn't solve many problems, and creates some intractable ones.

I find myself calling her an ape.

References:

   Abitbol MM. 1995. Reconstruction of the sts 14 (Australopithecus africanus) pelvis. Am J Phys Anthropol 96:143–158.

   Harrison T. 1986. A reassessment of the phylogenetic relationships of Oreopithecus bambolii. J Hum Evol 15:541–584.

   Harrison T. 1991. The implications of Oreopithecus bambolii for the origins of bipedalism. In: Coppens Y, Senut B, editors, Origine(s) de la bipédie chez les hominidés, Cahiers de Paléoanthropologie. Paris: Editions du CNRS. p 235–244.

   Köhler M, Moyà-Solà S. 1997. Ape-like or hominid-like? the positional behavior of Oreopithecus bambolii reconsidered. Proc Natl Acad Sci U S A 94:11,747–11,750.

   Lovejoy CO, Cohn MJ, White TD. 1999. Morphological analysis of the mammalian postcranium: A developmental perspective. Proc Natl Acad Sci U S A 96:13,247–13,252.

   Lovejoy CO, Simpson SW, White TD, Asfaw B, Suwa G. 2009a. Careful climbing in the Miocene: The forelimbs of Ardipithecus ramidus and humans are primitive. Science 326:70e1–70e7.

   Lovejoy CO, Suwa G, Simpson SW, Matternes JH, White TD. 2009b. The great divides: Ardipithecus ramidus reveals the postcrania of our last common ancestors with African apes. Science 326:100–106.

   Lovejoy CO, Suwa G, Spurlock L, Asfaw B, White TD. 2009c. The pelvis and femur of Ardipithecus ramidus: The emergence of upright walking. Science 326.

   Robinson JT. 1964. Adaptive radiation in the australopithecines and the origin of man. In: Howell FC, Bourlière F, editors, African ecology and human evolution. London: Methuen and Company, Limited. p 385–416.

   Rook L, Bondioli L, Köhler M, Moyà-Solà S, Macchiarelli R. 1999. Oreopithecus was a bipedal ape after all: Evidence from the iliac cancellous architecture. Proc Natl Acad Sci U S A 96:8795–8799.

Sarich VM. 1971. A molecular approach to the question of human origins. In (P. Dohlinow & V.M. Sarich, Eds.) Background for Man: Readings in Physical Anthropology, pp. 60‐81. Boston: Little, Brown.

Sarmiento EE. 2010. Comment on the paleobiology and classification of Ardipithecus ramidus. Science 328:1105. doi:10.1126/science.1184148

   White TD, Asfaw B, Beyene Y, Haile-Selassie Y, Lovejoy CO, Suwa G, WoldeGabriel G. 2009. Ardipithecus ramidus and the paleobiology of early hominids. Science 326:75–86.

White TD, Suwa G, Lovejoy CO. 2010. Response to Comment on the paleobiology and classification of Ardipithecus ramidus. Science 328:1105. doi:10.1126/science.1185462