A. africanus

Recent University of Michigan Ph.D. Jeremy DeSilva gets some nice press about his work demonstrating that fossil hominins didn't climb like chimpanzees:

"Frankly, I thought I was going to find that early humans would be quite capable, but their ankle morphology was decidedly maladaptive for the kind of climbing I was seeing in chimps," DeSilva told LiveScience. "It kind of reinvented in my mind what they were doing and how they could have survived in an African savannah without the ability to go up in the trees."

This is a good example of the comparative method in paleoanthropology. We can't observe the behavior of extinct species; we can only observe the behavior of their living relatives. We can observe the anatomy of fossil specimens, but testing hypotheses about their behavior requires us to understand the relationship between anatomy and behavior in living species. We've known about the anatomy of fossil hominid ankles for a long time, but it's not so obvious how the anatomical differences between them and chimpanzee ankles relates to behavior.

I've followed the literature on early hominid diets from the beginning of the weblog. In 2005 I discussed Peter Ungar's analyses of dental occlusal morphology in A. afarensis versus Homo, concluding:

The contrast between Homo and A. afarensis is in the same direction as the contrast in occlusal morphology between primarily meat-eating carnivores like felids and canids as opposed to more omnivorous carnivores like bears. Another observation is that meat is a major food resource of chimpanzees, although this is hardly a fallback resource. Indeed, if meat eating was indeed an important component of the behavioral repertoire of early Homo, it probably is not fair to assert that the difference in diet between Homo and Australopithecus was primarily a difference in fallback resources. It may be true that australopithecines and early Homo overlapped in their food resources, particularly in plant species consumed. But considering the likely effectiveness of early humans as predators, I think it likely that the fallback foods of early humans--when hunting was ineffective--may well have been the preferred foods of australopithecines. And when australopithecines were forced to abandon their preferred foods by early humans, they were forced to fall back upon resources that either were common or were difficult for early Homo to exploit. The disappearance of early small-bodied Homo by around 1.6 million years ago, and the ultimate extinction of the robust australopithecines after a progressive increase in their molar sizes (Wood and Lieberman 2001) indicate that this fallback strategy could not be maintained in the face of increased hunting effectiveness by large-bodied Homo.

The concept of "fallback foods" has captured a large mindshare in explaining early hominid diets. The idea is that a species may depend on preferred, staple foods for most of the year, but adopt less preferred, "fallback" foods when their staple is not available -- for instance, during the dry season.

What can fallback foods explain about early hominids? For one thing, they could explain the difference between robust and non-robust australopithecines. We know from isotope data (reviewed in this 2005 post about Matt Sponheimer's work) that A. africanus and A. robustus had similar fractions of C₃ and C₄ plant source foods in their diets. Across the year, they may have eaten roughly the same mix of foods. A 2005 paper by Greg Laden and Richard Wrangham (discussed here) explored the idea of underground storage organs of plants, or tubers, as fallback foods for australopithecines. Later studies of isotope data using laser ablation of small segments of the enamel (discussed here) showed that diet proportions may have substantially varied across the time that teeth were developing -- possibly concordant with the idea of seasonal or longer-period fallback foods. An earlier analysis of dental microwear in the two hominids by Scott and colleagues (discussed here) came to a similar result: there was great variability in wear properties, especially within A. robustus, although the average in the two species showed a possibly greater fraction of brittle, hard foods consumed by the robust australopithecines.

So I've written about the topic a lot, and followed it closely.

Now, Peter Ungar, Frederick Grine and Mark Teaford have examined the wear properties of the molars of Australopithecus (Paranthropus) boisei. They find that -- unlike A. robustus -- none of the seven specimens showed any evidence of having eaten hard or brittle foods:

Comparisons with the extant baseline series suggest that none of the Paranthropus boisei individuals examined consumed extremely hard or extremely tough foods in the days before death. All of these specimens lacked the extremes of Asfc evinced by Lophocebus albigena and especially Cebus apella, both known to consume hard, brittle foods. Paranthropus boisei molars also lacked the extremes of epLsar seen in Trachypithecus cristata and Alouatta palliata, both known to consume tough leaves and stems. The P. boisei individuals examined evidently avoided such metabolically challenging foods, at least in the days before death. This is notably consistent with Walker's [23] early assertion that P. boisei microwear patterns resemble those of living frugivores, and differ from those of living grazers, leaf browsers, and bone feeders.

Comparisons with the South African hominins suggest that while Paranthropus boisei may have consumed foods with similar ranges of toughness as those eaten by Australopithecus africanus, the eastern African "robust" hominin did not eat harder and brittler foods than the South African "gracile" form. Further, the patterns for P. boisei and P. robustus are very different. Paranthropus robustus likely ate foods that were on average much harder and less tough than P. boisei. The differences in both central tendencies and ranges of variation suggest different feeding strategies, and by implication, that the two species of Paranthropus probably had markedly different diets or foraging strategies (Ungar et al. 2008, italics lost).

That is very interesting that A. robustus and A. boisei are so different in their microwear patterns. It makes me wonder whether there may have been substantial habitat variation in the use of hard foods -- maybe the extant A. robustus sample, mainly drawn from a small area of South Africa, had access to some food items that were rare or absent across the larger East African range of A. boisei. But if some A. boisei populations had also depended on such hard resources some of the time, you might expect that we would have found one, or at least a bit more variability. Yet the sampled specimens, drawn from a distance from Ethiopia to Tanzania and well over a half million years of time, are pretty uniform in their microwear, showing some variability in the anisotropy dimension (here, high values have mostly parallel striations, attributed to fibrous food consumption).

So we can return to the question: the major hominid competitor of A. boisei was Homo. Both lineages appeared in the period around 2.5 million years ago, and remained sympatric throughout the next million years. Some of the dynamics of that interaction must have involved diet (considering the different dietary adaptations of the two). We can speculate that A. boisei didn't get much meat, which would then be an important difference. But what else was A. boisei eating?

Meanwhile, the data are still consistent with the idea of fallback foods in A. robustus as a driver of dental morphology, but the story for A. boisei now seems less clear. With only seven specimens, there is almost certainly not enough data to test the hypothesis -- which after all predicts that the use of hard brittle foods may be rare. But that's not positive evidence either. Is there some other food that might explain the hyperrobust craniodental morphology?

References:

Ungar PS, Grine FE, Teaford MF (2008) Dental Microwear and Diet of the Plio-Pleistocene Hominin Paranthropus boisei. PLoS ONE 3(4): e2044. doi:10.1371/journal.pone.0002044

I've been trying to spread the interviews across the field in various directions. I (virtually) talked with Mica Glantz about Neandertals, Adam Van Arsdale about early Homo, and Anne Weaver about human brain evolution, all the australopithephiles in the readership are probably feeling neglected.

So I wrote to Michelle Drapeau, who was very generous in answering questions about her work on the anatomy of early hominids and her recent field work in Ethiopia. Michelle is on the faculty of the Université de Montréal, in the Department of Anthropology. She serves as co-director of field operations in the Bala Paleoanthropological Research Area of southern Ethiopia.

Hawks: I will start out by asking about your dissertation work, which centered on the new partial skeleton from Hadar, A.L. 438-1. How did you get involved in that analysis?

Drapeau: It's a case of being at the right place at the right time. Bill Kimbel and Don Johanson had asked my advisor at the time, Carol Ward, to describe all the postcranial material recovered from the field in Hadar since 1990. Among those specimens was the partial skeleton of A.L. 438-1 which included associated fragments of the humerus, clavicle, radius, right ulna, mandible, and frontal as well as a complete left ulna, right and left second metacarpals and left third metacarpal. Considering the relatively numerous body parts from one individual, Carol thought the specimen deserved a more detailed analysis. I was Carol's Ph.D. student at the time and the 438-skeleton (as we started to call it) appeared like an ideal subject.

Hawks: What did you have to learn to be able to undertake the work?

Drapeau: I had to learn a lot! My master's thesis was in the history of science field, so all the functional anatomy, including the descriptive and comparative aspects were completely new to me. It was something I really wanted to do, however, so I really enjoyed immersing myself into it.

Hawks: A.L. 438-1 exhibits more curvature across its length than A.L. 288-1, an issue that you discussed in your analysis of the fossil. I have always been puzzled by the problem of ulna curvature -- mainly because I've always been puzzled by the comparison of later, larger, and more curved fossils like Omo L40-19 and OH 36 -- and then, of course, KNM-WT 15000 is a lot more like most recent humans. Do you have any insights about these contrasting morphologies?

Drapeau: Forearm bone curvature is an intriguing issue. Intuitively, it makes sense to assume that curvature reflects arboreality since the curvature of both the ulna and radius give greater area on the interosseous membrane for attachment of forearm muscle important for arboreal locomotion such as the finger flexors. However, orangutans and gibbons do not have the most curved forearm bones. It is an honor that goes to gorillas, definitely not the most arboreal animal of the bunch. If the area of muscle attachment is the variable that interests us, then it is important to take into account forearm length as well. When that is done, species generally sort by locomotor preference, with the most arboreal having the greater ‘area' for muscle attachment relative to body size and humans having the smallest (at least, when measured on the ulna). So gorillas appear to have very curved forearm bones because they also have relatively short forearms when compared to other apes.

The differences between A.L. 438-1 and A.L. 288-1 are fairly minor and probably reflect normal within-species variation. Neither is very curved and they may belong to a population with slightly more curved ulnae than modern humans but definitely less curved than any extant apes.

The KNM-WT 15000 specimen is pretty much what you would expect an ulna belonging to a completely terrestrial biped to look like, i.e., it is not particularly curved. Since it is a juvenile, it is difficult to compare it to other fossils, but there is nothing really surprising about it.

That said, what about the intriguing Omo L40-19 and OH 36? These specimens present combination of morphologies that are difficult to underscore in quantitative analyses. The former had a human-like proximal morphology but a really long and curved (ape-like) diaphysis. The latter, OH 36, has a general ape-like morphology with a pronounced curvature, but is unique in a few characters. The whole bone (proximal articulation and diaphysis) is very constricted medio-laterally, more comparable what is observed in monkeys (and it is not the result of distorsion). Despite its general ape-like morphology, it has an olecranon process that projects proximally like no other ape of its size. It is definitely much more human-like for that trait and it is generally agreed that it is a hominin. McHenry and colleagues argue in a recent article (AJPA, 134: 209-218) that these two fossils are very different and can hardly be accommodated into the same genus (Paranthropus) as it is usually done (probably by default). McHenry and colleagues argue that it may indicate Paranthropus is in fact a polyphyletic taxon. They also conclude, as I stated above, that OH 36 is unlike anything living today.

So, if curvature of the ulna reflects arboreality, does it mean that these fairly recent fossils were much more arboreal than A. afarensis? Remember that they are big ulnae, particularly L40-19, likely belonging to large individuals.... Maybe the Paranthropus clade (if indeed it is a clade) is more arboreal than A. afarensis? This would imply either reversal of behavior or that A. afarensis is not ancestral to Paranthropus. Or, alternatively, could the curvature in these individuals reflect forelimb muscularity but not necessarily related to arboreality? As you can see, I have many more questions than answers. All this variability suggests that the behaviors of fossil hominin species were much more variable than what we have been used to think and may have been (very?) different from the behaviors of extent species.

Hawks: Of course, the big debate about forelimb proportions is the idea that they may have been very different (and more apelike) in A. africanus compared to A. afarensis. (reviewed by Green, Gordon, and Richmond 2007) What do you think about the issue?

Drapeau: That idea first met with some resistance because it involved a reversal of proportions from A. afarensis to A. africanus and implied a more arboreal behavior in the latter than the former. Given that Homo habilis is often described has having more ape-like proportions than A. afarensis, it also implied that A. afarensis may not be the ancestor of the Homo lineage (an idea more recently suggested by Yoel Rak and colleagues based on mandibular data). Since I remain unconvinced of the primitive proportion of H. habilis, I am not so certain that the 'derived' proportions of A. afarensis exclude it from being an ancestor to the Homo lineage.

Back to the differences between the two australopithecine species. Despite original skepticism, the data appears to be robust and the differences in joint size between A. afarensis and A. africanus appear to be real. As observed in the previous question, this variability may reflect locomotor differences possibly related to differences in the environment. If A. afarensis was still occasionally arboreal, is it too hard to imagine that, if the environment is changed (more wooded, greater predator pressure, more resources found in trees, etc.), the percentage of arboreal behavior would increase and that the proportions would revert to being more chimp-like in A. africanus? Again, there is no reason to assume that all early hominins, because they were bipedal, were identical in their locomotor behaviors.

I want to underscore that these differences are in joint SIZE, not in limb length, and reflect relative loading of the limbs. Usually, the major source of loading of the limbs is related to locomotion, but it is an assumption that cannot be verified in early hominins. If, as stated above, OH 36 is unlike anything living today, maybe it did things that have no modern equivalent. And the same can be said of other hominin species including A. africanus with its 'apparent' primitive proportions.

Hawks: You have recently been involved in field research in the Bala-Weyto region of southern Ethiopia. Can you describe the site, and your role?

Drapeau: The Bala–Weyto basin is part of a series of small parallel rifts that link the northern limit of the East African Rift to the southern limit of the Main Ethiopian rift. These small rifts constitute today a string of many small basins. The Bala-Weyto basin is located east of the Omo river basin. It is a region more difficult to survey when compared to dryer region because of the vegetation coverage that limits exposures visibility and access. However, it is little-explored paleoanthropologically speaking. Work in the Konso, another small basin a few kilometers away, but at a higher altitude, has a fauna with a certain degree of endemism and an A. (P.) boisei specimen with unique morphological variations. Among other things, we want to know if this variation and the faunal endemism are due to the relative isolation of the basin or to its particular environment. These answers may be found in contiguous basins that vary in their physical characteristics, such as the Bala-Weyto basin.

I am co-director of that project with Elizabeth Harmon of the City University of New York. At this stage of the project, being co-director involves organizing the whole expedition, securing funding, and coordinating the work of other team members. I would say that the most time consuming aspect is coming up with money and getting everything moving in the field. As a director, I am responsible for the team's well-being and it is a pressure that can sometimes weigh heavily on my shoulders. It is nice to be able to share the burden with a co-director.

Hawks: Do you involve students in your work?

Drapeau: My funding is limited and field work in Ethiopia is not particularly cheap. However, I plan to bring one student in the field this summer. I look forward to share this experience with a highly motivated student!

Hawks: Many of us have heard about the difficulties of field research, particularly in East Africa. What are some of your biggest challenges?

Drapeau: Doing field work in Ethiopia can be a challenge for many reasons. As can be expected, there are numerous permissions, letters, official documents, etc., that are required and the bureaucracy is somewhat heavy. However, I find Ethiopians very helpful and professional and, usually, the quest for documents goes smoothly, particularly once you know what to do and in what order.

A second difficulty is the access to the sites. Ethiopia did not have one highway until relatively recently and road traveling remains an experience that can be frightening. A lot of work is being done on the roads, however, and I believe that things will keep improving. Access to the research area involves off-road traveling as well, with all the difficulties that it entails. When you leave for the field, you have to be a self-sufficient unit, relying on the local environment as little as possible. It is still necessary to get gasoline on a regular basis, but except that, we try to be as autonomous as possible. It is particularly important when you go to a new area and don't know what (if anything) will be available to you.

A third aspect of field work, particularly in Ethiopia, is the politics, the paleoanthropological politics that is. Although most scientists are polite and civilized to each other, I really feel that we had to walk on eggs when we were researching an area in which to conduct field work.

A final difficulty (and certainly not the least) in our situation, is to find an area that has fossiliferous exposures of a time period that interests us and in which we can work at least a few years. The numerous discoveries that are made in East Africa give the impression that finding hominin fossils is something easy to do, but it usually involves many years of surveying. We are still at the exploratory phase of our project, i.e., we are still actively looking for an area that could sustain scientific work for a few years. Hard work (and perhaps a little luck) is essential.

Hawks: You had a lot of field experience before going to Ethiopia. How did you get your start?

Drapeau: At the end of my undergraduate degree, I had the chance of getting a couple of paying jobs in prehistoric archaeology. It was the beginning of a series of jobs in field archaeology conducted in parallel to my studies. I used to think (and still do) that these were the best summer jobs an anthropology student could have. The pay check was very descent and it usually came with room and board. These jobs allowed me to see many regions of Quebec and Canada that I would otherwise have never visited and to do things I would probably have never done otherwise. I have flown in helicopters for hours (and even survived a major crash), piloted a hydroplane (just for a few minutes, but still!), hear wolves howl into the night while trying to sleep in a tent hundreds of miles from any road or civilization, dipped my foot in the arctic ocean (too chicken to swim), seen the midnight sun, and I could go on. This fieldwork experience, and a stint in the Caune de l'Arago in Tautavel, France, opened another door: to be invited to do field work in Hadar in 2000.

Hawks: Any interesting stories?

Drapeau: I have an anecdote that I find amusing, but mostly informative on the nature of humans. When we were doing field work in the Bala basin, our camp was set up about a 2-hour drive off the road. It was clear that the local people had seen very few foreign workers. For the whole time we were there, we had a constant group of people just sitting in the shade observing us like zoo animals, watching our every move, laughing when we did things unexpected, etc. We were quite the entertainment. The occupation of the local Mali people appeared to be tending their few sorghum fields, but mostly to take their sometime large herds of cows, goats and sheep a few miles down to the river for a drink every day. Even though it was not that hot, the men walk around wearing only colorful underwear (the Speedo-type) and it was sometimes literally falling apart. From our western perspective, they really seem to have almost nothing. Anyhow, after a few days in the field, some crew members were starting to crave fresh meat. We agreed to allow the cook to purchase one goat from a local herder. We didn't think it would be a problem given the large quantities of these animals around and our willingness to pay a fair price for it. It came as quite a surprise that no one was willing to sell us any! It turned out that goats, sheep and cows were not herded to be eaten or even milked, but were really just status items. One man from the village nearby apparently owned more than a hundred head of livestock but was still unwilling to sell. We were all quite shocked of the apparent frivolity of it all, particularly considering that food (for humans and beasts) did not appear to be particularly abundant in the region. But then, we couldn't miss seeing the connection to what we can observe in the western world: huge houses for one or two people, oversized and overpriced cars. These are just to show off. The same frivolities, although expressed slightly differently, can be found anywhere. I guess it really is in the human nature. We were finally able to convince someone to sell us a goat, but we paid a really high price.

Hawks: Congratulations! You seem to be a very busy person right now, both professionally and personally. What's next for you?

Drapeau: I just started one of the most challenging projects of my life, a project that will keep me busy for the rest of my life. His name is Henri and he is almost 8 months old. Professionally speaking, I am investigating manipulatory adaptations in the early hominin hands and the morphology of muscle markings. However, one of my main objectives in the next two years is to settle on a specific field research area with good scientific potential.

It's that time of year again -- the time when those boring ``Year in Review'' magazines are on newsstands, and when pundits make fools of themselves predicting what will happen in the next year.

Well, I'm not too proud to join the fools, as I've shown the last two years. In 2006, I got five predictions right out of ten. Not bad for my first outing, but you'll see that last year's predictions fared even better:

• 10. Sahelanthropus postcrania will be published. I'm frankly shocked that this didn't happen. I don't doubt the rumors, but I'm starting to wonder whether this story is more interesting than it looks....
• 9. Two words: Holocene evolution. OK, this was a little unfair, considering that my work was an important part of making this prediction come true. Still, Discover made ``recent human evolution'' one of its top 100 science stories of the year, even before our December paper came out -- mainly on the strength of the paper by Scott Williamson and colleagues from earlier this year. And "Human genetic variation" was Science's "Breakthrough of the Year" -- most of that variation representing recent evolution.
• 8. Despite (or because of) the success of the Neandertal genome project, there will be no genetics of any kind published on early modern skeletal material. Puzzling, isn't it? But then, considering the trouble with Neandertal contamination reported in August, maybe we're better off leaving the early Upper Paleolithic alone for a while.
• 7. The mitochondrial history of human dispersals will become more and more detailed, but no paper will test against other loci. D'oh! Reading this one a year later, it's pretty obvious that I should have included Y chromosome in this one, since those two get compared all the time! Proofread, Hawks!
• 6. Another (yes, another) paper about the chimpanzee-human divergence will peg it between 5 and 7 million years ago. Will they never tire of these? Hobolth et al. (2007, PLoS Genet 3:e7) pegged the divergence at 4.1 million years. That's too recent to fit my prediction. Instead, I have to turn to Ebersberger et al. (2007, Mol Biol Evol 24:2276), who placed the divergence at 5.7 million years ago. Both estimates are too recent for Sahelanthropus, which the geneticists have started to figure out....
• 5. Three papers with new Ethiopian fossils. The last few years, one annual Ethiopian find seemed to be predictable enough. So I figured, why not three? We got a not-nearly-noted-enough paper this summer by Gen Suwa and colleagues descringing the Konso Homo erectus remains. Then, Suwa brought us Chororapithecus -- hey, I didn't say "hominid!" That's two. But despite the long-ago announcement of the Woranso-Mille skeleton, its appearance in a meetings abstract and a mid-summer press release about further Mille fossils, all we got from the peer review system is a lousy faunal list. Well, the faunal list does include the hominids. Should it count as a "paper with new Ethiopian fossils?" I'll say yes -- hey, unlike Aramis, at least the Mille fossils are new!
• 4. Another early Upper Paleolithic specimen will emerge from a museum collection. The only bizarre thing about this one was the location: South Africa. Hoffmeyr may not be that convincing as a European early Upper Paleolithic skull, but it was sure sold that way. Weird.
• 3. A big year for Miocene apes, which will look increasingly important in the story of human brain evolution. No brains, but it sure was a big year for Miocene apes, with two significant East African discoveries claiming to push back the timeline of African ape divergence.
• 2. Maturation rate in early Homo becomes a dead issue, because of the variation in dental and skeletal maturation in living people. Wishful thinking. Still, did Tanya Smith (2007) breathe new life into perikymata? Let's just say that unresolved questions remain.
• 1. The year will end without a single new hominid species having been named. This one was like dodging a bullet, since new species riffle out of paleoanthropologists' minds all the time. From 2001 to 2006, there were six (six!). In 2007, none.
• BONUS: A dramatic development in the problem of pre-2.0-million-year-old Homo. Rats.

OK, that's seven out of ten. It's beyond belief that I did better in the top five than the bottom five -- I picked those because they were far out there. I mean, really -- a new Upper Paleolithic specimen from a museum collection? After Muierii, that's like calling lightning to strike twice. But there it is, and in January, no less.

I'm clearly going to have to pick stranger predictions this year. And I'll have to be careful about that "dramatic development" line -- I mean, it's appropriately Delphic, but what is it supposed to mean, really? I wonder whether "operatic development" might be better.

And do I dare call down my non-lightning strike for a third year? It's ruining my percentage! It's starting to reek of desperation -- I mean, it starts to look like the stopped watch effect even if it happens.

Oh, well. I mean, those are just the risks of predictions, right? Suppose in the preseason I had picked Kansas to win the Orange Bowl!

• 10. A dramatic development in the Sahelanthropus story.
• 9. Both major-party candidates for the 2008 U.S. Presidential election will accept evolution.
• 8. This year's featured piece of anatomy: the femur.
• 7. No new hobbits, at least, not from Flores.
• 6. An incisive example of introgression in East Asia.
• 5. A viral insertion in the human genome will tell us about a disease of the australopithecines.
• 4. Another language gene joins FoxP2. No word on whether Neandertals have the human version.
• 3. Homo habilis: an endangered species?
• 2. This year, something new from three A's: A. afarensis. A. africanus. Atapuerca.
• 1. Oh, and one more A. Ardipithecus.
• BONUS: A big, big year for Neandertals. I mean, besides the election.

There you have it. I'm not sure which of these is the riskiest, but I'm sure they're more out on a limb than last year!

Raymond Dart (p. 198 of Australopithecus africanus, the man-ape of South Africa, Nature 115:195-199, 1925), summing up why hominids might have lived in what seemed "harsh and forbidding" environments for a primate:

In anticipating the discovery of the true links between the apes and man in tropical countries, there has been a tendency to overlook the fact that in the luxuriant forests of the tropical belts, Nature was supplying with profligate and lavish hand an easy and sluggish solution, by adaptive specialization, of the problem of existence in creatures so well equipped mentally as living anthropoids are. For the production of man a different apprenticeship was needed to sharpen the wits and quicken the higher manifestations of intellect -- a more open veldt country where competition was keener between swiftness and stealth, and where adroitness of thinking and movement played a preponderating role in the preservation of the species. Darwin has said, "no country in the world abounds in a greater degree with dangerous beasts than Southern Africa," and, in my opinion, Southern Africa, by providing a vast open country with occasional wooded belts and a relative scarcity of water, together with a fierce and bitter mammalian competition, furnished a laboratory such as was essential to this penultimate phase of human evolution.

Just noticing, in this John Noble Wilford article:

A new report, to be published Thursday in Nature, will review more skeletal evidence of the transitional aspects of the Dmanisi specimens.

More later...

UPDATE(2007/09/18): Wilford doesn't directly state the article's theme but it clearly has one: Why the heck can't these people agree about these fossils that have been out of the ground for thirty years?

The first answer that everyone has given him is about the "million year gap" between 3 million and 2 million years ago. People can't agree about early Homo because they can't decide what its ancestors looked like. Without any ancestors, they don't know which of the traits of early Homo are derived.

For a good example, we can turn to a feature Wilford doesn't mention: limb proportions. Recently, a lot of ink has been spilled discussing the evolution of arm size in later australopithecines and early Homo. OH 62 (probably Homo habilis) and A. africanus have been argued to have large arms compared to their legs. A. afarensis and Nariokotome (KNM-WT 15000, probably Homo erectus) have relatively small arms compared to their legs. Did H. habilis and H. erectus have different ancestors? Did H. erectus evolve from H. habilis, reverting its limb proportions to earlier A. afarensis? Or are all these comparisons just batty, since only three specimens have arm and leg elements whose length can be compared? There's no clear answer; but one of the most important specimens in the question (with sort-of-intermediate limb proportions) is the Bouri skeleton, BOU-VP 12/1, which at 2.5 million years old is right in the middle of that "gap."

The more you look at the "gap," the less gap-like it looks. For one thing, we have a pretty good idea of what was going on behaviorally during that million year span. The first stone tools are 2.6 million years old. The technology of these toolmakers -- although simple -- included all the basic manufacturing methods used before 1.5 million years ago. The tools were used to butcher animals and break bones for marrow; so we know that the toolmakers were depending on meat.

Second, we actually have quite a lot of fossils from this time period. The entire South African A. africanus fossil record, with the exception of a few early specimens like STW 573, come from this "gap." A fairly extensive record of the appearance and evolution of early robust australopithecines comes from this time period in East Africa.

And, here and there, a few specimens look Homo-like. Wilford's article discusses AL 666-1. To this we can add the Uraha mandible, Omo 75-14, an additional series of teeth from Omo, and possibly the Bouri BOU-VP 35/1 skeleton.

Properly considered, the rarity of early Homo in these contexts is not a problem; it is information. Wilford quotes Philip Rightmire to this effect, and we can easily expand on the basic concept. Early toolmakers did not undergo an immediate geographic expansion upon their origin. They spread across a relatively narrow strip of East Africa and stayed there for more than a half-million years. They were initially rare. That means that their adaptation was not immediately a barnburner of a success -- the early toolmakers took a while to perfect the adaptation of later Homo.

The middle part of the article takes in another reason for disagreement: whether H. habilis and H. erectus were ancestor-descendant:

Several scientists, notably Dr. White of Berkeley, took issue with the interpretation seeming to imply that evidence for the two species overlapping in time and exhibiting variable sizes was new. That, he said, had been recognized for a couple of decades.

Dr. Kimbel, who was not involved in the new research, defended the authors, saying that they had not "meant to imply that habilis could not have been ancestral to erectus, presumably on the basis of their being contemporaneous at Turkana," the site in Kenya where the fossils were found.

Susan C. Anton, an anthropologist at New York University who was a member of the Spoor-Leakey team, said, "My money is still on habilis as the potential ancestor, but there is a lot of room for additional knowledge, given the dearth of fossils."

None of these statements really disagree with each other. If anything, this particular question may have gotten easier to resolve lately, not as a consequence of new fossils, but as a result of new dates for many of the old ones. Susan Anton is later quoted saying that anagenesis "is the only option that is no longer on the table," and it seems to me that this is the clearest statement most likely to invite some hypothesis testing. But it is fairly clear that this problem cannot be resolved in terms of earlier fossils: I don't think there's any compelling evidence of H. erectus before 1.6 million years ago.

There is one significant word that doesn't appear in the article -- an absence that is especially interesting considering the quoted scientists:

Kenyanthropus

Remember, the dominant theme is about complexity and bushiness. And yet, here's that forgotten branch of the family tree; the one that was supposed to clarify everything by providing a different ancestor for KNM-ER 1470 from other H. habilis specimens, the one that showed a distinct line leading to Homo originating in the Early Pliocene.

I think our bush may have been pruned.

In case you're following the debate about Homo habilis limb proportions, there's a new contribution by Martin Haeusler and Henry McHenry in the JHE holding pen. They examined the partial KNM-ER 3735 skeleton.

KNM-ER 3735 is often assigned to Homo habilis, but it's not exactly an easy diagnosis. There are a few pieces of the skull preserving anatomy, including the cheek, frontal and temporal. Here's what Bernard Wood (1991) had to say about the skeleton:

The form of the mandibular fossa and malar region virtually preclude this specimen from being attributed to A. boisei. Its general affinities are with Homo. Some features (e.g. vault thickness) ally it with a Homo erectus-like hominid, but in other areas (e.g. the frontal) it is more like crania such as KNM-ER 1813, a conclusion endorsed by Walker (1987) and by Leakey et al. (1989). Tobias (1989) includes KNM-ER 3735 within H. habilis.

Provisional taxonomic assessment: Homo sp. indet.

Well, that's not exactly a rousing endorsment. You can see the problem --- and it's a common tale for hominid fossils. It has a smaller brain than early H. erectus (that would be the "frontal looks like KNM-ER 1813 bit). But its cranial bones are thick. The most complete of the bones in the skeleton is a radius, but it's not complete. The best bone for estimating joint surface area is the sacrum; a femur shaft is there, but it falls short of the midshaft length.

And there's a problem: the radius seems pretty big, but the sacrum is little. If it were a human, the radius looks like it came from a body twice the size of the sacrum. There's something going on here. Previous work has assumed that the sacrum is more likely reflective of the size of the body, and the radius is therefore big compared to a small body mass. Maybe that means more climbing, leading to a greater role in weight support for the arms. Or maybe it means a retention of more apelike proportions.

This is a frustrating literature to follow, because pretty much every other early specimen except Lucy (AL 288-1) and the Nariokotome skeleton (KNM-WT 15000) present exactly the same problem. You can't estimate limb sizes very accurately from small pieces of bone. And you can't estimate proportions accurately at all without estimates of size. Plus, it's not clear that you can interpret limb proportions without a decent estimate of body mass. Two years ago, there was a huge go-around about the limb proportions of OH 62. Like KNM-ER 3735, it looks to have a relatively large arm compared to its body. Or maybe the legs are short. Or maybe the estimates are bad. You get the picture. So everybody has a different clever statistical transformation to try to make these fossils comparable to each other. I have no argument with any of the work; but it seems like the error involved in these assessments of proportions is pretty large relative to the information content of the bones.

Here's some of the conclusion from Haeusler and McHenry:

Our analyses suggest that the idea that KNM-ER 3735 had more primitive body proportions than A.L. 288-1 (e.g., Leakey et al., 1989) needs to be refined. We found a unique but distinct mosaic of modern and ape-like limb proportions in the two early hominid species. H. habilis shares a gracile humerus and radius and a small base of the hand phalanges with the earlier A.L. 288-1 and modern humans. In addition, other characteristics, including the relatively small size of the sacrum and a robust midshaft of the phalanges, are common to both early hominids and extant great apes. Surprisingly, however, those upper limb proportions that differ between the two fossil species, such as a robust scapula, a long radial neck, and a long forearm, are all more ape-like in H. habilis.

In KNM-ER 3735, the shoulder muscles that originate on the scapula (trapezius, deltoid, supraspinatus, and infraspinatus) as well as the biceps brachii were, therefore, probably not only more powerful than in modern humans, but also stronger than in A.L. 288-1. On the other hand, the extraordinarily short lever arm of A.L. 288-1's biceps muscle, the minute elbow size, and the small radial head may indicate a weaker arboreal component in its behavioral repertoire than in H. habilis. However, in the absence of modern correlates, caution is needed with respect to possible behavioral implications of the different forearm proportions in the two species.

They also note the Homo-like anatomy of the femur shaft, including a marked pilaster.

Seth Dobson (2005) claimed that that the sacrum of STW 431 (A. africanus) is also small -- it certainly yields a small mass estimate compared to other elements of the skeleton. Heck, all of the early hominid sacra yield small mass estimates. Well, you can see it's confusing.

References:

Haeusler M, McHenry HM. 2007. Evolutionary reversals of limb proportions in early hominids? Evidence from KNM-ER 3735. J Hum Evol (in press) doi:10.1016/j.jhevol.2007.06.001

Dobson SD. 2005. Are the differences between Stw 431 (Australopithecus africanus) and A.L. 288-1 (A. afarensis) significant? J Hum Evol 49:143-154. doi:10.1016/j.jhevol.2005.04.001

I'm about two-thirds of the way through Mike Morwood's new book, The Discovery of the Hobbit, and I'll be posting a review when I'm through. Generally, I have a positive opinion of the book so far.

Henry Gee has reviewed the book in this week's issue of Nature. I wanted to point out my generally positive attitude about the book, so that you'll know that my miserable opinion of Gee's review has little to do with the book's merits.

Consider how Gee starts his review:

The unicorn, wrote Jorge Luis Borges (in Kafka and His Precursors), is universally regarded as a supernatural being of good omen. But there's a problem: despite its folkloric familiarity, we wouldn't know how to recognize a unicorn if we met one in real life. It "does not figure among the domestic beasts, it is not always easy to find, it does not lend itself to classification," Borges continues. "It is not like the horse or the bull, the wolf or the deer. In such conditions, we could be face to face with a unicorn and not know for certain what it was."

Is Gee smoking crack? What kind of blather is this?

First of all, I know I'm being terribly literal, but a unicorn is a horse with a horn. One horn. Not so hard to recognize! Maybe my 3-year-old daughters could help edit at Nature.

Let's see, where have I seen one of those that Gee might recognize? Oh, yeah:

Photo credit: Simon Stratford (via stock.xchng)

There it is, sound as a pound.

Next, Gee spends several paragraphs expositing on his own role in the publication of the Homo floresiensis announcement. We learn some interesting little facts, like how the authors wanted to name the species "Sundanthropus floresianus" until a reviewer pointed out that future students would confuse the name with a flowery butt.

I kid you not. Nature has a layer of reviewers to take tushie references out of taxonomy. Somehow they can't tell a left femur from a right, but they're on the watch for sphincter-species!

The review is entirely self-serving -- there are only three paragraphs that include any reference to the book! In the midst of this babbling about unicorns and hobbits, Gee tells us that skepticism at new hominid discoveries should be dismissed as the predictable result of "mindsets" of the skeptics:

Such reaction is common in the wake of new hominid discoveries, which are routinely dismissed either as pathological humans (Homo neanderthalensis) or apes (Australopithecus africanus and Sahelanthropus tchadensis). Such reactions say less about the facts than the mindsets of commentators, who might be unwilling to have their comfortable views of the world so forcibly changed. Confronted with what might be a genuine unicorn, many would prefer to see a pantomime horse with a spike glued to its head.

Ooooh! Since I'm one who has been notably skeptical of Sahelanthropus and have approached H. floresiensis skeptically, I'm obviously a prime target for this paragraph. It is so comfortable to stay in my view of the world where hominids interbreed with each other. Clearly, a bestiary that includes small-brained island bipeds must shake me out of my comfort zone.

How could I have been so wrong! When every species ever proposed has faced the same resistance? Sure, Tim White says that Kenyanthropus is a glued-together matrix-filled A. afarensis, but that's just his mindset. Or how about Eoanthropus? Sure, Franz Weidenreich thought that it was just a concoction by "English authors," but couldn't he tell that it was more than just a pantomime skull with an orangutan jaw? Why couldn't I see that these petty minds were just holding back the important work of taxonomy!

No, no, no. You see, if we approach things skeptically, we won't dare to dream about the unicorns:

The unicorn remains as it always did, frustratingly elusive. This year, the researchers will return to Liang Bua to see if they can discover more. But stories such as this demand a mythological beast altogether less serene. It is as if the researchers had set out to discover some new form of fossil mouse, only to find that they had grabbed a dragon by the tail instead. And as any devotee of Harry Potter will remind you: Draco dormiens nunquam titillandus.

The theme of the review is perhaps to be expected from Gee, otherwise known as the author of The Science of Middle-Earth. But I find his mixture of fantasy and science to be especially malaprop in the context of the Flores fossils, since with every fantasy word he detracts from the credibility of the journal's review process!

Some of you will have seen the episode of The Simpsons, titled "Lisa the Skeptic," where Lisa excavates an "angel" from the ground. Here's part of the synopsis from Wikipedia:

As Homer attempts to get a motor boat, a new shopping mall in Springfield is being built on an area where a large number of fossils were found. Lisa condemns and protests the building of the mall. Thanks to her protest, it prompts the school to conduct an archaeological dig. When Lisa is digging, it reveals a human skeleton with wings. Springfield's residents are convinced it is an angel, and Homer cashes in by moving the skeleton into the family's garage; however, Lisa is skeptical, believing it may not actually be an angel, and even has Stephen Jay Gould test a sample of the skeleton. The next day, Dr Gould runs to the Simpson house and said the tests came out inconclusive and after Lisa on television compares belief in angels to belief in unicorns and leprechauns, Springfield's religious zealots riot and destroy all of the scientific institutions.

Later, we find out that the "angel" is a publicity stunt for the new mall; Guest voice Gould confesses that he never really performed any tests on the "angel". This is one of my favorite episodes: it's a rare one where Lisa's preachy skepticism is entirely justified, and the "expert" doesn't care enough to do anything at all.

Now I know, that the episode was missing a scientific editor to encourage Lisa to forget about her doubts, and just to accept the "angel" for what it is. After all, every new discovery has its skeptics.

Well, there is a lesson to take away from all the unicorn talk. If you are in Cardiff and find the skeleton of a giant, be sure to send your report to Nature, where you'll find a receptive editor. Despite what they may say, there's not one of those born every minute.

UPDATE (4/26/2007): A reader e-mails, "Remember that Borges was blind." True. Perhaps we can extend this analogy further?

Another reader: "Well, at least we can expect a fair set of reviews on the Sahelanthropus postcrania...D'oh!"

References:

Gee H. 2007. In a hole in the ground.... Nature 446:979-980. doi:10.1038/446979a

Sponheimer and colleagues (2006, link) zapped some Swartkrans teeth with lasers to measure their ¹³C content. I wrote quite a bit here last year about australopithecine diets, including a long review of isotopic evidence for australopithecine diets.

With respect to dietary differences between A. africanus and A. robustus (the two species with any substantial isotopic sampling), there are four essential observations:

1. The apparent C_{4 dietary content of the two species is basically the same, and fairly high.}
2. High C₄ foods are not so easy to come by, they include some grasses and sedges and the animals who eat them.
3. The Sr/Ca ratios of the two species are fairly different.
4. The postcanine teeth of A. robustus seem to be adapted to crushing and grinding, moreso than A. africanus.

One hypothesis for the difference in Sr/Ca ratios is exploitation of underground tubers (warthogs and mole rats have elevated Sr/Ca similar to A. africanus). A mix of C₄ foods has been proposed to solve the grass-eating problem, including seeds, rhizomes, insects, lizards, and herbivore meat. But these don't really solve the postcanine tooth conundrum, and while they may both be true; neither is really testable.

OK, so does the new laser ablation study solve any problems? First, let's read a bit about what exactly it is, and why it might be useful. Ann Gibbons has written a ScienceNOW article:

[A] team of American and British researchers studied the teeth of four individuals of Paranthropus robustus (also known as Australopithecus robustus) from the Swartkrans Cave in South Africa. The team scanned the teeth with a sensitive laser, which did not destroy the teeth but etched them lightly enough to free carbon gases long trapped in the enamel. Because different plants absorb atmospheric carbon dioxide differently, the researchers were able to see what types of vegetation the hominids ate based on the ratio of carbon isotopes in their teeth.

An accompanying perspective by Stanley Ambrose explains:

In contrast to conventional methods, the laser ablation technique used by Sponheimer et al. barely penetrates the enamel surface of an area of less than 0.5 mm² and is thus nearly nondestructive (2). Laser ablation also avoids the problem of time averaging in large drilled grooves. Moreover, perikymata can be counted, providing a good estimate of the minimum time interval sampled and of the duration of tooth formation.

The Paranthropus teeth studied by Sponheimer et al. show interesting patterns of seasonal variation in diet and climate. All have the isotopic composition of mixed feeders, and two show at least ca. 40% variation in the proportions of C3- and C4-based resources over 1 year. One individual had a predominantly C3-based diet and foraged in a cooler, more humid environment; it may have formed its tooth in a very wet year. The others ate more C4-based foods in a warmer, drier environment. Their average carbon-isotope ratios are similar to those of adaptively versatile savanna baboons (2). Analyses of seasonal variation in teeth of modern and fossil baboons and of other hominin species are necessary to evaluate dietary specialization in Paranthropus and niche overlap with other hominin species.

Back to me. There are two possibilities. First, the differences between ¹³C values for different samples might be sampling the actual dietary variability of single A. robustus individuals over the course of their tooth development (in this paper, sampled over a course of a couple hundred days).

Or second, they may just be sampling noise.

The paper presents comparative data to suggest that this is actual variability in diet and not isotopic noise. They sampled some steenbok teeth from Swartkrans with the same technique. Steenbok are consistent C₃ browsers; their diet doesn't vary much in its ¹³C proportion over time. And the samples from the steenbok teeth didn't show very much variation across different sampling zones from the same tooth. Hence, it looks like the samples from different perikymata actually may give a consistent picture of dietary ¹³C composition over time.

Compared to the steenbok, the A. robustus samples show great heterogeneity in ¹³C content. This heterogeneity is manifested when looking at multiple samples from the same tooth, and it is also manifested when looking at different individuals. So far, that would seem to indicate dietary heterogeneity -- the A. robustus individuals ate a different mix of foods over time, and different individuals ate different foods.

On the basis of the magnitude of difference (particularly within the single specimen SKX 5939), Sponheimer et al. propose that some individuals must have gone from a diet predominantly composed of C₃ foods to one predominantly C₄ within the span of two years (estimated 644 days).

Here's how their paper concludes:

A dental microwear study of the earlier (3.0 to 3.7 Ma) hominin Australopithecus afarensis found no evidence that its diet changed over time or in different habitats (20). In contrast, stable carbon isotope (3, 4) and dental microwear texture analyses (1) of the slightly younger (3.0 to 2.4 Ma) hominin A. africanus demonstrated that its diet was far more variable. This suggests the possibility that a major increase in hominin dietary breadth was broadly coincident with the onset of increasing African continental aridity and seasonality after 3 Ma (21, 22) and only shortly antedated the first probable members of the genera Homo and Paranthropus (23-25) and the earliest stone tools (26). The undoubted toolmaker Homo is thought to have been a dietary generalist that consumed novel foods such as large ungulate meat and tubers that are abundant in savanna environments (27-30). Paranthropus, in contrast, with its extremely large and flat cheek teeth, thick enamel, robust mandible, and heavily buttressed facial architecture, is often portrayed as a dietary specialist (27-29). Further, it has been argued that this specialization contributed to its extinction when confronted with increasingly dry and seasonal environments later in the Pleistocene, whereas Homo's generalist adaptation was crucial for its success (28, 29). Our results suggest that Paranthropus had an extremely flexible diet, which may indicate that its derived masticatory morphology signals an increase, rather than a decrease, in its potential foods. Thus, other biological, social, or cultural differences may be needed to explain the different fates of Homo and Paranthropus (31).

We have lots of other reasons to believe that robust australopithecines were not dietary specialists, as pointed out by Wood and Strait (2004). Robust australopithecines had broad geographic ranges, were able to disperse over long distances, and persisted despite substantial climatic and environmental changes. The evidence for dietary differences across the lifespan is certainly consistent with this.

It does, however, make for an interesting conundrum: if australopithecines were selected on the basis of their ability to find different foods over the course of years, that suggests a strong role for social learning of more food types and broader geographic ranges. But if this was the path taken by robust australopithecines, what was the path taken by Homo?

References:

Ambrose SH. 2006. A tool for all seasons. Science 314:930-931. DOI link

Gibbons A. 2006. Not just nuts and berries for these hominids. ScienceNOW 9 Nov. Full text

Sponheimer M, Passey BH, de Ruiter DJ, Guatelli-Steinberg D, Cerling TE, Lee-Thorp JA. 2006. Isotopic evidence for dietary variability in the early hominin Paranthropus robustus. Science 314:980-982. DOI link

Wood B, Strait D. 2004. Patterns of resource use in early Homo and Paranthropus. J Hum Evol 46:119-162. DOI link

Rex Dalton has a great two-page article in Nature about the bush vs. ladder dispute. It keys off of the Middle Awash Australopithecus anamensis article by White and colleagues from a couple of weeks ago.

If you recall that one, White et al. posited that Ardipithecus was likely ancestral to Au. anamensis, and that the two did not overlap in time. Here's the key exchange in the Dalton piece:

This month's Nature paper makes a bold argument, and shows the Awash team seeking to put its mark on the record. Others in the
field are impressed. "When you find 30 new hominid fossils, you are allowed a certain amount of conjecture," says Bernard Wood, a palaeoanthropologist at George Washington University in Washington DC. "As always, they have done a fantastic job."

But he and others are unconvinced by the Awash team's conclusion: "This is only the first half of the rugby match," says Wood. Meave Leakey, lead author on the Au. anamensis discoveries in Kenya, is more blunt. "I don't believe this," she says. "We do not have the specimens to fill the gaps."

Leakey and Wood are among those who believe that other, as yet undiscovered hominid species may have lived at this time, from 4.4 million to 2.9 million years ago. The existence of other species would cloud or eliminate the argument for a direct lineage. "My prejudice is there are more lineages rather than fewer -- more diversity," says Wood. "I have to concede these new data are dramatic. But we should beware coming out with a complete explanation when we don't have all the
evidence."

This argument frustrates White. "There were Martians there back then too," he says. "And spacecraft all over the Pliocene -- we just haven't found them yet."

Waiting for Monte Cassino

In a series of articles since 2000, White and colleagues have laid out a systematic attack on the "bushy" phylogeny model. Their arguments have extended across four million years and seven species, with a breadth that rivals the Allies breaking the Winter Line.

Consider the angles of attack:

1. Au. anamensis -- Au. afarensis. Everyone basically accepts that Au. anamensis is a direct ancestor of Au. afarensis. And the two species are really not very different from each other -- for instance, they are more alike than either is to Ardipithecus. The transition between these species would look to be a simple case of anagenesis, except...

...for Kenyanthropus (Leakey et al. 2001). This small-toothed, flat faced hominid needs an ancestor, too. Au. anamensis might have been the common ancestor of Kenyanthropus and Au. afarensis. If so, then both these later species originated by cladogenesis from Au. anamensis. A similar argument might be made for other species, like Australopithecus bahrelghazali (Brunet et al. 1996) or the Sterkfontein Member 2 hominids. But Au. bahrelghazali is only known from a partial mandible and only differs from Au. afarensis by a three-rooted premolar, which is considered by many to be weak evidence, and the Sterkfontein Member 2 sample has not yet been taxonomically assigned -- they might turn out to be Au. afarensis, for example. Kenyanthropus remains the strongest case for cladogenesis (i.e., a "bush"). Yet...

...White (2003) denied that the Lomekwi skull KNM-WT 40000 was a distinct species. In particular, he argued that the extensive postmortem deformation of the skull made it impossible to substantiate an anatomical difference from Au. afarensis, and even if it was different, the anatomical diversity of living hominoid species is so great that it would probably encompass the difference between KNM-WT 40000 and known Au. afarensis crania.

2. Earliest hominids. At the moment, the earliest putative hominids include three genera: Orrorin (Senut et al. 2000), Sahelanthropus (Brunet et al. 2002), and Ardipithecus, represented in the Late Miocene by Ar. kadabba (Haile-Selassie 2001, Haile-Selassie et al. 2004). Evidence for obligate bipedality has been challenged (by different researchers) for each of these three (I'm one of those who has questioned bipedality for Sahelanthropus).

So far the only comparable anatomical parts from all three samples are teeth...

...which were examined by Haile-Selassie, Suwa and White (2004). They concluded that the variation among these three genera

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 (Haile-Selassie et al. 2004:1505).

Additionally, Ohman, Lovejoy and White (2005) challenged the interpretation of the internal anatomy of the Orrorin femur, which had been suggested to be more derived than that of Au. afarensis. They wrote:

We agree that the Lukeino femur's external morphology suggests some form of bipedality. Yet the more detailed original scans appear to show a distinct superior cortex different from Australopithecus and humans, with the cortex distribution being more primitive than that seen in any other hominid, including Australopithecus.

The relevance of this argument to the phylogenetic diversity of early hominids depends on the anatomy of the Ardipithecus femur, which none of the rest of us are in a position to know. But one may speculate that if all these early "hominids" had femora with similar morphology, it would further reinforce the interpretation that they belong to a single lineage.

3. Ardipithecus -- Au. anamensis. This is the current example. Here's how Dalton discusses it:

The latest Afar discovery is exciting experts because it shows that the three hominids existing in the same area, but in successive time periods. Tim White of the University of California, Berkeley, co-leader of the Awash team, believes this points to a direct lineage between the three -- a process called phyletic evolution. The new Au. anamensis fossils are only 300,000 years younger than Ar. ramidus, meaning that if one became the other, the changes would have had to happen that fast. But the key point, says White, is that fossils of Au. anamensis and Au. afarensis have never been found in sediments the same age as those containing Ar. ramidus. If fossils of the different species were found together, that could show that they belonged to multiple lineages existing simultaneously.

Finding remains of all three species in the same area but not from the same time period suggests they did not coexist, says White.

...

The specimens also provide anatomical clues to evolutionary history. "The new Au. anamensis fossils are anatomically intermediate between the earlier Ar. ramidus and the later Au. afarensis," says White. For example, the teeth of the newly discovered Au. anamensis fossils seem adapted to chew tougher and more abrasive foods than Ar. ramidus. The researchers believe this shows that Au. anamensis had a broader diet. "All this strengthens the view that there is phyletic evolution from Ar. ramidus through Au. anamensis," says White. He believes he has nailed down the relationship between the two later species, although he says that further specimens are needed to prove the earlier link (Dalton 2006:1100).

Of course, it would help matters if we knew in more detail what Ardipithecus looked like. But one must imagine that the stage is being set for its revelation. The unilineal interpretation places Ardipithecus at the critical point as an ancestor to the major mid-Pliocene australopithecine lineage. Extending the unilineal interpretation earlier into the Late Miocene would make Ardipithecus the earliest hominid as well.

It is not necessary to think that taxonomic uniformity means anatomical uniformity, though. Ardipithecus already encompasses a trend of decreasing canine size and less sectorial P₃ for example. A trend toward fuller skeletal adaptation to bipedality may also be imagined. But in that context, it is important to note that the time interval between the Orrorin femur and the unpublished Aramis skeleton is longer than the time between Aramis and Hadar. Those relative times may become quite important in thinking about the evolution of those postcrania.

The Winter Line was broken at Monte Cassino, after many failed attempts from different approaches. The Aramis fossils are either the heavy shoe waiting to drop, or they are the uncomfortable foot that all this talk about phyletic evolution is meant to shoehorn into place.

Commentary

If all these cases are added together, they imply a single evolving lineage encompassing at least four anagenetic taxa, Ar. kadabba -- Ar. ramidus -- Au. anamensis -- Au. afarensis. This last would presumably be followed by a cladogenesis into a robust australopithecine species (Australopithecus aethiopicus) and Australopithecus africanus.

One could add Homo erectus to this list, since White and colleagues argued in their description of the Daka skull (Asfaw et al. 2002) that the Asian and African samples represent one cosmopolitan species.

But then one species sticks out as a surprising exception to the pattern: Australopithecus garhi (Asfaw et al. 1999). It will be interesting to see a close argument showing why this species is really different from South African Au. africanus. Say, more different than KNM-WT 40000 is from the Hadar crania. It's quite glaring, really, that this species should be there mucking up such a simple phylogeny.

I have to say, after reviewing all these papers in one sitting -- this entire bush vs. ladder thing is getting very tiresome! I mean, isn't there something else that we could organize early hominid discoveries by? These are all papers in the top journals, and this is the (fairly specialized) discussion that has been promoted as the central issue in the field!

The subtitle of the Dalton piece suggests that it is merely a philosophical difference:

Deciding whether our ancestors evolved as a single lineage may depend more on philosophy than fossils.

But that's not really true. There is a clear null hypothesis here, quite directly drawn from William of Ockham:

entia non sunt multiplicanda praeter necessitatem

Which of course means:

Sometimes fossil samples really do form ancestor-descendant relationships.*

(*) It doesn't really. It means "Entities should not be multiplied beyond necessity."

References:

Asfaw B, Gilbert WH, Beyene Y, Hart WK, Renne PR, WoldeGabriel G, Vrba ES, White TD. 2002. Remains of Homo erectus from Bouri, Middle Awash, Ethiopia. Nature 416:317-320. DOI link

Asfaw B, White T, Lovejoy O, Latimer B, Simpson S, Suwa G. 1999. Australopithecus garhi: A new species of early hominid from Ethiopia. Science 284:629-635. DOI link

Begun DR. 2004. The earliest hominins -- is less more? Science 202:1478-1480. DOI link

Brunet M. and 37 others. 2002. A new hominid from the Upper Miocene of Chad, Central Africa. Nature 418:145-151. DOI link

Brunet M, Beauvillain A, Coppens Y, Heintz E, Moutaye AHE, Pilbeam D. 1995. The first australopithecine 2,500 kilometres west of the Rift Valley (Chad). Nature 378:273-275. DOI link

Dalton R. 2006. Feel it in your bones. Nature 440:1100-1101. DOI link

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

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

Leakey MG, Spoor F, Brown FH, Gathogo PN, Kiarie C, Leakey LN, McDougall I. 2001. New hominin genus from eastern Africa shows diverse middle Pliocene lineages. Nature 410:433-440. DOI link

Ohman JC, Lovejoy CO, White TD. 2005. Questions about the Orrorin femur. Science 307:845. DOI link

Senut B, Pickford M, Gommery D, Mein P, Cheboi K, Coppens Y. 2001. First hominid from the Miocene (Lukeino formation, Kenya). Comptes Rendus 332:137-144.

White T. 2003. Early hominids -- diversity or distortion? Science 299:1994-1996. DOI link

Tim White and colleagues (2006) report on new fossils from Aramis and a new site, Asa Issie, with estimated dates between 4.1 and 4.2 million years ago.

In addition to the paper, there are articles in the New York Times (by John Noble Wilford), the Associated Press (by Seth Borenstein), and BBC (by Paul Rincon).

The story is being played as another "missing link" -- this one between Ardipithecus and Australopithecus. From the Times:

Tim D. White, a paleontologist at the University of California, Berkeley, who was a leader of the team, and his colleagues said the 4.1-million-year-old fossils were anatomically intermediate between the earlier species Ardipithecus ramidus and the later species Australopithecus afarensis, the Lucy family. The newfound bones and teeth are the earliest remains of the most primitive Australopithecus, known as anamensis.

"This new discovery closes the gap between the fully blown australopithecines and earlier forms we call Ardipithecus," Dr. White said in a statement. "We now know where Australopithecus came from before four million years ago."

The fossil specimens are a partial maxilla from Aramis, ARA-VP-14/1; two partial maxillary dentitions from Asa Issie numbered ASI-VP-2/2 and ASI-VP-2/334; and a large femur shaft fragment, ASI-VP-5/154. There are also several postcranial bones -- phalanges, vertebrae, a metatarsal -- that are pictured in some of the press accounts and briefly discussed but not pictured or numbered in the paper. The postcanine teeth in the maxillary specimens are larger than the known sample of Ardipithecus, but the canines are larger and more mesiodistally elongated than in Australopithecus afarensis. The best anatomical match for these features is with the Kanapoi and Allia Bay samples assigned to Australopithecus anamensis, and White and colleagues assign the new fossils to that species.

So why are these fossils important? On the surface, there isn't very much to them. Three piecemeal upper dentitions don't tell much. They have big molars and big canines, both within the range of Au. anamensis. Neither they nor the femur shaft extend the known range of variation in early hominids.

Remembering that every fossil fragment is a precious relic of a bygone age, the main importance of these is that they may address hypotheses about the biogeography of Early Pliocene hominids. The maxillae show that a large-molared hominid existed in the same geographic location at a later time than the small-molared Ardipithecus. That could be interesting, and it is the hook for the news stories and the team's press statement.

The strongest part of this story is the geographic -- finding them in the Middle Awash instead of Kenya -- and the paleoenvironmental. There is some suggestion in the paper that there may be a paleoenvironmental difference at the sites that currently have evidence of Au. anamensis:

Palaeoenvironmental circumstances surrounding Au. anamensis ~1,000 km to the south in Kenya have been described for Allia Bay as a mixed assemblage sampling aquatic, forest, grassland and bushland. Nearby Kanapoi conspecifics were found in another mix of environments described as dry, possibly open, wooded, or bushland conditions with a wide gallery forest in the vicinity. Habitat preferences in such mixed assemblages are difficult to ascertain despite the assertion that the hominids "favored mosaic settings". In contrast, the Ethiopian occurrence of Au. anamensis described here allows its tight spatial and temporal placement in a vertebrate assemblage with taphonomic integrity. Its relative abundance suggests that it was a regular occupant of a wooded biome that appears to have persisted in this part of the Afar during the 200,000-yr interval subsequent to Ar. ramidus at Aramis (White et al. 2006:887-888).

This points to two salient facts about the Australopithecus lineage: they were able to disperse effectively across relatively long distances, and occupy at least those habitats where wooded cover and resources were available.

On the other hand, the fossils don't really "fill a gap" between Ardipithecus and Australopithecus, because they are pretty firmly within the time range of known Au. anamensis, being around the same age as the Au. anamensis sample from the Lake Turkana area -- the oldest Kanapoi hominids may be between 4.1 and 4.2 million years old also. The paper points out the other East African examples of Australopithecus at or above 4 million years ago; but it omits the Sterkfontein Member 2 remains, which are also conceivably in the age range of Au. anamensis. Or, for that matter, the Lothagam mandible, which might be the earliest australopithecine even if its date weren't as high as the >5 Ma estimate.

The paper attempts to close off -- for the moment -- the idea that there were allopatric species of early (ca. 4 Ma) australopithecines with differing dietary adaptations. But the paper cannot reject this hypothesis without caveats:

Two phylogenetic hypotheses concerning the origin of Australopithecus can be offered to account for the available data. The first hypothesis derives Au. anamensis phyletically from Ar. ramidus within a 200,000-yr interval [i.e., between 4.4 and 4.2 Ma]. The second involves cladogenesis of Au. anamensis from an ancestor (presumably Ardipithecus or some close relative) even deeper in the Pliocene or Late Miocene. Under the latter hypothesis, Ar. ramidus would represent a relict species in an ecological refugium (White et al. 2006:888).

This latter alternative is the only "bushy" interpretation -- the idea that known species of Ardipithecus can't really be the direct ancestors of Australopithecus, but that there must be some as-yet-undiscovered hominid (or better yet, hominids) that are the common ancestors, cousins, and other bushy relatives of the known species. White and colleagues cannot reject it, but they clearly do not favor it.

In its place, they suggest Ardipithecus ramidus as a lineal, possibly anagenetic ancestor of Au. anamensis, and Au. anamensis as the anagenetic ancestor of Au. afarensis. It's a ladder from primitive to derived, small-molared to big-molared, big-canined to small-canined.

I tend to think this is the null hypothesis -- we have sampled adaptations that differ because of evolution in what is essentially a single lineage of successive species. I say "essentially" because there was not necessarily a wholesale transformation of one species to another across its entire range. Instead, dispersals of new adaptive packages by population movements were probably important biogeographic aspects of evolution in these early hominids. But I think it important to recognize that one species can indeed be the ancestor of a later species.

People who like their phylogenies bushy and their speciations punctuated can take solace in that 200,000-year gap. The finding of Au. anamensis within the already-known time range of Au. anamensis means that the new fossils haven't really added much to the question of phylogenetic diversity in early hominids.

As a postscript, I have a nomination for "most significant sentence" in the paper:

At Aramis, the lone hominoid and largest primate was Ar. ramidus (109 of 6,156 identified specimens so far) (White et al. 2006:888, emphasis added).

References:

White TD and 21 others. 2006. Asa Issie, Aramis and the origin of Australopithecus. Nature 440:883-889. DOI link

The paper by Guatelli-Steinberg et al. (2005), earlier referred to here, is now available online from PNAS.

The results are basically as reported by National Geographic, finding that Neandertal anterior teeth have perikymata counts within the range of living human populations. Perikymata are microscopic ridges on the enamel surface of teeth; they mark the incremental growth of the teeth over small periods of time. The idea has been that these ridges work a bit like tree rings; they mark the amount of time that the tooth took to grow. However, as this study indicates, the formation of perikymata is not quite so simple as the addition of tree rings, and human populations actually vary substantially in the number of perikymata on their teeth.

What makes this different from earlier work (like Ramirez Rossi and Bermudez de Castro 2004) is the inclusion of an African sample. The very low perikymata count of the recent Africans significantly extends the range, which had previously been assessed in Europeans only. Thus, the conclusion here is that there is no evidence from perikymata to indicate that Neandertal development was any different from that within living human populations.

Now we can wait for the other shoe to drop:

The finding from the African population sampled here shows that some developmentally normal humans have much lower perikymata counts than others. This varies by tooth (since they don't all develop for the same time): the lower canines have the highest counts, with a mean over 150; the lower incisors have the lowest counts with a mean down near 100. Remember that these values are means; individuals in the sample must have scored lower, although the range of the sample is not reported in the paper.

With this sample, the human range encompasses the Neandertals. It encompasses all the earlier European hominids (chiefly from Atapuerca) sampled by Ramirez Rossi and Bermudez de Castro (2004), because these hominids had counts higher than Neandertals.

Let's take a look at Dean et al. (2001:628), who give values for earlier hominids. Here's a table including some earlier hominids along with the South African values from Guatelli-Steinberg et al. (2005). The current paper does not include the numbers, so I am reading estimates off the figure, but considering they are means and the important aspect is the total range, the numbers aren't critical. Lower numbers are less like the recent Europeans that were the standard before the new comparative work.

From these numbers, Sangiran 4 and SK 27 are within the range of modern human population means. So are three of the teeth of Australopithecus (i.e. A. africanus), and the remaining three teeth are pretty close, so that it seems likely the A. africanus dentition wasn't very different in its perikymata number from the range of living Africans.

The standouts are KNM-WT 15000 and Paranthropus (i.e. A. robustus). A. robustus is easy to explain: its anterior teeth are a lot smaller than ours. A lot smaller. If enamel formation rates were similar, then they ought to have taken less time to form, regardless of other aspects of somatic development.

The puzzle is KNM-WT 15000, the famous Nariokotome skeleton. Is this skeleton a normal representative of early human populations? Is it at the extremely low end of a normal range including others like KNM-ER 1590 (also a bit smaller than the mean, although probably not outside the range of living Africans)? Is it pathological?

The other shoe is the research paper that will cover all these questions.

Now it could be that these numbers really aren't comparable for some reason; I don't do perikymata, but I can tell that the counts depend on estimates of crown height and packing density, so it's not obvious that they were derived in the same way (although the papers do share one author).

But the Neandertals are far from the most interesting part of this perikymata problem. Can we tell a human from an australopithecine from these data? If so, why do some of the earliest humans have the lowest (i.e. sub-australopithecine) counts?

I think we can disregard the idea that their somatic development rates were "highly derived" in a non-human-like direction. It's not like they're Neandertals, after all.

References:

Guatelli-Steinberg D, Reid DJ, Bishop TA, Larsen CS. 2005. Anterior tooth growth periods in Neandertals were comparable to those of modern humans. Proc Nat Acad Sci USA 102:14197-14202. Abstract

Dean C, Leakey MG, Reid D, Schrenk F, Schwartz GT, Stringer C, Walker A. 2001. Growth processes in teeth distinguish modern humans from Homo erectus and earlier hominins. Nature 414:628-631.

Ramirez Rossi FV, Bermudez de Castro JM. 2004. Surprisingly rapid growth in Neanderthals. Nature 428:936-939. Full text (subscription)

From a new paper by Greg Laden and Richard Wrangham:

We propose that a key change in the evolution of hominids from the last common ancestor shared with chimpanzees was the substitution of plant underground storage organs (USOs) for herbaceous vegetation as fallback foods. Four kinds of evidence support this hypothesis: (1) dental and masticatory adaptations of hominids in comparison with the African apes; (2) changes in australopith dentition in the fossil record; (3) paleoecological evidence for the expansion of USO-rich habitats in the late Miocene; and (4) the co-occurrence of hominid fossils with root-eating rodents. We suggest that some of the patterning in the early hominid fossil record, such as the existence of gracile and robust australopiths, may be understood in reference to this adaptive shift in the use of fallback foods. Our hypothesis implicates fallback foods as a critical limiting factor with far-reaching evolutionary effects. This complements the more common focus on adaptations to preferred foods, such as fruit and meat, in hominid evolution.

Tubers are not the only kinds of USOs; there are also corms, bulbs, and rhizomes. I tend to use "tuber" as an easier-to-type version of USO, though. I was practically dared to review the paper here (nota bene: I do respond to dares, albeit more carefully and slowly than for most things), and Carl Zimmer has also written a short item on the idea. The mole rats are the lede, but there is much more to it than them, and in many respects they are the least problematic part.

So here is my semi-rambling take.

Take one

In 1999, Wrangham and Laden, along with David Pilbeam, James Holland Jones, and NancyLou Conklin Brittain, suggested that tuber cooking was central to the adaptation of early Homo. The evidence for that suggestion was and remains essentially absent. As Henry Bunn put it in his comment to the paper:

Why is there abundant evidence of hunting and some form of scavenging, carcass transport, butchery, and sharing and consumption of meat and fat in the behavioral and dietary adaptations of early Pleistocene Homo (e.g., Oliver, Sikes, and Stewart 1994 and references therin)? Why are the earliest stone tool kits of the Oldowan dominated by sharp-edged cutting tools? Why is there intensive meat polish on the edges of stone flake knives studied for microwear (Keeley and Toth 1981)? Why is there not microwear evidence of grit or sediment damaged on the teeth of supposedly tuber-feeding hominids themselves, including the robust australopithecines (Kay and Grine 1988)? (Bunn 1999:580)

Additionally there is the problem of the complete lack of evidence for cooking and the weakness of evidence for early control of fire, compared to the strong and substantial evidence for both much later in the Pleistocene.

So early Homo just doesn't show any signs of having been a serious tuber-eater. Not to say it is impossible; just that there isn't any particular evidence for the idea.

Take two

Now, Australopithecus, that's another story. Robust australopithecine teeth in particular have a lot of pits and scratches on them, as if they were eating some hard, gritty foods. Underground storage organs fit that bill. Eating a lot of dirt along with them might well explain the high rate of dental wear that robust australopithecines clearly had -- many had their first molars worn almost completely flat before the third molars came into occlusion.

In this context the fallback food idea seems like an especially good one. The tooth anatomy and microwear evidence indicate that robust and nonrobust australopithecines probably did not differ in most of their dietary spectra, but instead in the accentuation of different food sources that were shared by both. If food shortages were important in the evolution of these hominids, one way that the difference between them might have been sustained was an ecological difference in fallback food utilization. Hominids like A. afarensis and A. africanus undeniably had teeth adapted to heavy grinding, fracturing off brittle foods, and intensive attrition compared to any other living or fossil primate. So it makes no sense to propose that the difference between these "gracile" australopithecines and later robust australopithecines was that the "gracile" ones lacked the high-chewing element. Rather, it makes considerably more sense to suppose that both kinds of hominids were eating the high-chewing foods, with the robust ones making a more intensive use of them, and possibly lacking some of the tough pliable foods eaten by earlier nonrobust species. A difference in fallback strategies might comprise exactly this kind of dietary prediction.

To me, the coolest thing about the hypothesis is that it explains the postcanine adaptations of australopithecines without reference to the now-well-known carbon isotope data. Indeed, the question of C₄ versus C₃ foods is entirely irrelevant. I discussed the carbon and other stable isotope data in an earlier post; the short story is that all kinds of australopithecines appear to have included around a 25 to 30 percent component of C₄ foods, which include grasses, some sedges, and the animals who ate them.

Peters and Vogel (2005) proposed that the C₄ component of the early hominid diet could be explained as a sum of several different plant and animal sources, including around 5 percent each of seeds, roots and pith, insects, small mammals and vertebrates, and large mammal meat. That does a good job of describing a diversified hominid diet without reference to tubers.

But the thing about USOs is that relatively few of them are C₄ plants. If hominids did eat tubers, in other words, they still wouldn't account for the C₄ fraction of the overall diet.

However, they might account for the postcanine dental adaptations of later hominids, under the assumption that they represent a substantial part of the C₃ fraction. And the replacement of C₃ fruits by C₃ tubers would explain why robust and nonrobust hominids both have approximately the same C₄ fraction, while differing so greatly in their dental adaptations and dental microwear.

As far as I can tell, nobody has mentioned this implication, but it should be the next thing to test.

The evidence

But although I think Laden and Wrangham's study has some interesting possibilities, I think the data is a bit short of where it needs to be. What about the four lines of evidence used by Laden and Wrangham? Are they to be believed?

The first thing to point out is that a reading of the paper finds little detail to go along with two of the lines of evidence. It is true that australopithecine teeth are not like ape teeth, and that robust australopithecines were different from nonrobust ones. The innovative suggestion here, although brief, is that an enlarged oral cavity in australopithecines, particularly robust ones, may be an adaptation to increase the exposure of masticated tuber to salivary digestion.

But the dental discussion appears less as two independent lines of evidence converging to one conclusion, and more as throwing up whatever seems relevant to see what will stick. A review of early hominid dental evidence also reveals plenty that is less consistent with the hypothesis that USOs were an important food for most early hominids.

For one, the comparative dental evidence is questionable. As Laden and Wrangham review the issue, Hatley and Kappelman originated the argument that the early hominid dentition was adapted to tuber-eating:

In 1980, Hatley and Kappelman pointed out parallels in dental morphology that suggested that bears, pigs, and hominids are all adapted to eating significant amounts of plant underground storage organs (USOs). They summarized their argument as follows: "We believe that postcanine similarities evident among ursids, suids, and hominids are in part an adaptation for processing this tough, fibrous, and gritty plant part. Bears, pigs, and humans are adapted to exploiting plant roots and tubers, although their methods of food gathering are functionally rather than morphologically analogous. Convergence upon the resource of belowground plant storage parts appears to make the responses of nonretractable claws, cartilaginous snout, and digging stick equivalent" (Hatley and Kappelman 1980:380, quoted in Laden and Wrangham 2005:1).

This isn't obviously true. For one thing, Pliocene pigs appear to have been mainly grazers (Harris and Cerling 2002 -- not cited by Laden and Wrangham 2005). They increased in molar size and complexity in several different lineages, as a reflection of their increased reliance on C₄ vegetation. The diet of current-day suids in particular seems to share little in common with early hominids, at least as far as their stable isotope ratios are concerned. Nor are large and flat early hominid molars particularly analogous to those of most bears -- perhaps the closest are pandas, which are far from dedicated tuber-eaters.

Then there is the problem with the earliest hominids. These, like the later ones, are found alongside mole rats, at sites like Aramis and Lukeino. But they don't have the postcanine adaptations of later hominids. The essential problem with the earliest hominids is not postcanine specialization, but instead the changing role of the canine-premolar complex, and the reduction of the canines. There is no reason (at least that I can think of) to suppose that small canines are adaptive to tuber-eating (and a search of the paper finds no occurrences of the word "canine").

One way to avoid this problem is to suppose that the USO-eating adaptation was simply a feature of later hominids --- say, A. anamensis and later. Perhaps it's true, but if so, the hypothesis loses some of its punch, and possibly one of the converging lines of evidence, since the expansion of USO-rich savanna central to Laden and Wrangham's paper starts in the Miocene.

And the paper would prefer to displace the importance of tubers earlier rather than later in time:

There is growing evidence that middle to late Miocene hominoids, mainly in Europe, exploited relatively open habitats, and may have exhibited dietary adaptations (Teaford and Ungar, 2000, Smith et al., 2003 and Smith et al., 2004) that we claim here to be related to USO consumption. This lends support to our assertions that a USO niche may have emerged during the Miocene, that this niche may have been important for non-fossorial mammals, and that certain features, such as thick enamel and large teeth, can arise in response to this niche. However, we do not wish to make claims beyond the hominid taxon at this time, other than to note that this may be a fertile area of future research (Laden and Wrangham 2005:13).

If you are a student looking for a thesis topic, don't pick this one.

The most original suggestion is that hominid and mole rat remains are significantly coassociated. On the surface, this looks like fairly convincing evidence that the hominids lived in USO-rich environments, which is precisely what Laden and Wrangham conclude. And indeed, the number of sites either possessing both kinds of animals or lacking both (27) is higher than expected considering the small number that have one kind but lack the other (11).

But wait a minute. Neither "mole rats" nor "hominids" are species, they are groups composed of several species. Let's consider the same kind of comparison for other kinds of animals. How many hominid sites lack bovids? Or suids? Or crocodilians? Keep in mind that some groups are rare at early hominid sites because they hadn't diversified yet, like papionins, or hadn't yet appeared in Africa, like equids. But these groups are found at many later hominid sites. And of course, for many sites the total species list may reflect less intensity of sampling rather than the paleohabitat.

In other words, the mole rats may show that hominids had the opportunity to eat USOs -- at least, if they could compete effectively with the mole rats for them. But they don't show that the hominids actually ate USOs. At least not if we aren't equally willing to believe that the presence of crocodiles at hominid sites meant that hominids swam in rivers and ate migrating wildebeest.

The weaknesses NOT mentioned

I see two significant weaknesses in the hypothesis. The first is the simpler of the two: digging up tubers is a lot of work.

For groups like the Hadza who eat a lot of them, this work takes many hours (at least by some group members). That kind of work seems unlikely for australopithecines, even hungry ones. Especially considering the full scenario: australopithecines digging intensively for savanna-living tubers for hours at a stretch would have been highly exposed to predation and heat stress for hours at a stretch.

Might they have done it if they had nothing else to eat? Sure. But could they have done so efficiently enough to get a net return on their effort? There's a question worth answering.

Might they have banded together into large defensive groups? Maybe, but that would seem likely to decrease foraging efficiency -- how many tubers are there in any small patch of ground? However, there is slight evidence for large multimale groups (chiefly AL 333), as well as pretty good evidence that predation was high and survivorship into adulthood low. Another question worth answering.

There may be a solution for this problem: perhaps the plants themselves have evolved under intensive hominid predation. Maybe today they put their roots further underground, or maybe the plants with tougher and more fibrous roots have predominated since the Pliocene. If so, australopithecines might have had an easier time of digging them up.

The other problem is more vexing. How can we demonstrate that an extinct species was adapted to eat a food that it did not eat very often? Bone chemistry must predominantly reflect the foods that make up the majority of the diet, not those that are consumed only intermittently. Microwear also ought to reflect the majority foodstuffs, although perhaps more weakly -- especially if mortality occurs mostly during periods of dietary stress, when animals are eating more of their fallback foods than usual. This is perhaps worth looking into.

Maybe the most promising test would be variability in tooth wear. Presumably the need to rely on fallback foods would vary in accordance with climatic conditions, on a multigenerational timescale. If so, then some individuals might exhibit relatively great amounts of attrition due to their reliance on fallback foods during long periods of resource stress, while other individuals might have lived in times of relative abundance, and therefore not have experienced significant amounts of wear. This kind of heterogeneity would itself have created differences in selection on tooth size, enamel thickness, and occlusal anatomy over time: perhaps in ways that could be differentiated from alternative strategies. But even so, that kind of comparison is relatively far from the direct evidence, and may be impossible with the fossil record we have available.

Summary

Looking back at the post, I've written a balance of critical comments and supportive ones. I guess my opinion overall is that the USO hypothesis is certainly worth presenting, but it has a ways to go before it is really testable. I think there is a balance of good ideas here and evidentiary weaknesses, and it is certainly worth talking about them, perhaps with a bit more skepticism and documentation than has yet been done.

And if you are serious about tubers, as Wrangham clearly has shown himself to be, then you are going to have to choose a time when they were important. With this paper, I have now read that tubers were the key adaptation for Miocene apes, the earliest hominids, australopithecines, robust australopithecines, early Homo, and recent humans.

It can't be all of these. If it were, they would all look the same. And there wouldn't have been any reason for one to change into anything else! So you have to pick.

And making a choice means more than saying, "well, Miocene apes tasted tubers, early hominids needed them when the fruit ran out, for australopithecines they were a fallback food, robust australopithecines ate them all the time, early Homo cooked them, and recent humans pickled them with vinegar and caraway seeds. As yet, the many tuber hypotheses have been just-so-storytelling at its most self-contradictory.

If I were picking, I would put the best odds on Laden and Wrangham's current argument: USOs were important fallback foods for nonrobust australopithecines like A. afarensis and A. africanus, and equally or more important for robust australopithecines. In contrast, early Homo was adapted to meat eating, and the earliest hominids -- who lack the postcanine specializations of later hominids -- remain as yet a mystery, although a fundamentally apelike diet is a good first guess.

This post doesn't account for all the details of early hominid diets, but some previous posts review other sources of evidence, including:

Stable isotope analyses

Dental microwear

Occlusal anatomy

References:

Hatley T, Kappelman J. 1980. Bears, pigs, and Plio-Pleistocene hominids: a case for the exploitation of belowground food resources. Hum Ecol 8:371Ð387.

Laden G and Wrangham R. 2005. The rise of the hominids as an adaptive shift in fallback foods: plant underground storage organs (USOs) and australopith origins. J Hum Evol in press (online)

Wrangham RW, Jones JH, Laden G, Pilbeam D, Conklin-Brittain N. 1999. The raw and the stolen: cooking and the ecology of human origins. Curr Anthropol 40:567-594.

Scott and colleagues (2005) examined dental microwear in some Swartkrans (A. robustus) and Sterkfontein (A. africanus) specimens. The interesting part of the study is the use of fractal analysis to quantify the complexity of scanned surfaces. They scanned a very tiny area of each tooth, around 200 micrometers on a side. Then they fed the scans through an algorithm to calculate texture.

The basic link to diet is the same as before: hard, brittle foods leave scars and pits, tough pliable foods leave directional marks like scratches.

Some results:

Fossil hominin results indicate that P. robustus (Asfc 4.29 2.150) has microwear textures more complex (chi-squared = 8.17, P < 0.005; Kruskal-Wallis test) and more variable in complexity (F = 16.82, P < 0.0005) than A. africanus (Asfc 1.686 +/- 0.52) (Fig. 2c, d). These results are consistent with the hypothesis that P. robustus incorporated more hard and brittle foods in its diet. However, some overlap in Asfc for the hominins (Fig. 3b) suggests that P. robustus was unlikely to have been a specialized hard-object feeder. It is more likely that hard, brittle foods were an occasional but important part of the diet. Previous studies have emphasized average differences between species rather than overlap, because low repeatability associated with observer error made assessments of within-species variability difficult.

In contrast, the microwear textures of Australopithecus africanus (epLsar1.8 0.0045 +/- 0.00163) show greater anisotropy (chi-squared = 3.84, P = 0.05; Kruskal-Wallis test) and epLsar variability (F = 7.38, P < 0.01) than P. robustus (epLsar1.8 0.0028 0.00060) (Fig. 2c, d). These data suggest a tougher diet on average for A. africanus compared with P. robustus, but one that is also more variable in its toughness (Scott et al. 2005:694).

The interesting thing is the overlap between the two samples. The authors also compared cebus and howler monkeys, finding extensive variation in both taxa, with minimal overlap in distributions (howlers are leaf-eaters, cebus eat a wider range of foods including some hard items). The two hominids overlap almost completely in "surface complexity" (i.e. whether they are pitted and scarred), with the main difference between the samples being an average greater complexity in A. robustus and an average greater anisotropy (i.e. grooving and scratching) in A. africanus. A third or so of each sample lie in the region of overlap in both variables.

From these measures, the diet variation within each species appears to be more extensive than the differences between them. The authors suggest this pattern of differences may represent a basically uniform diet with different fallback foods:

The greater variation in complexity for P. robustus and in anisotropy for A. africanus suggests that these species altered different components of their diet, but that there was probably substantial overlap in the fracture properties of their preferred foods. Thus, the clear differences between A. africanus and P. robustus microwear may relate, in part, to differences in critical dietary resources consumed only periodically during the year (Scott et al. 2005:695).

That would certainly be concordant with the stable isotope data. I guess it's a good thing for them that these two species weren't contemporaries.

References:

Scott RS, Ungar PS, Bergstrom TS, Brown CA, Grine FE, Teaford MF, Walker A. 2005. Dental microwear texture analysis shows within-species diet variability in fossil hominins. Nature 436:693-695. Full text (subscription required)

In a 2002 paper on cranial remains from Sterkfontein, Lockwood and Tobias write the following in a section called "Are there multiple hominin species from Sterkfontein Member 4?":

The Group C specimens (Stw 183 and Stw 255) arguably represent a phenon, as they deviate from the A. africanus sample in the same direction. Each exhibits some derived characters of A. aethiopicus, A. robustus, and/or A. boisei. Moreover, based on dental size and morphology, Stw 252 probably belongs in this group (Clarke, 1988).

Stw 183 is the strongest craniofacial evidence for a second species of Member 4, though it is not by itself definitive (Lockwood, 1997). Stw 183 is an immature individual, and a full interpretation of this specimen relies on a comparative framework of early hominin ontogeny that is at present incomplete. Despite its youth, it possesses characters typically found in A. robustus, such as an incipient maxillary trigon and a rounded lateral portion of the inferior orbital margin (not present in any other specimen from Sterkfontein Member 4).

The temporal bones catalogued at Stw 255 (including Stw 266a) resemble A. africanus in essentially one autapomorphic character: the prominent eustachian process. Otherwise, this individual shows traits corresponding to A. boisei, especially in the relationship of the tympanic to the postglenoid and mastoid processes. On the whole, Stw 255 suggests the appearance of the temporal bone in KNM-WT 17000 of A. aethiopicus. Moreover, Spoor (1993) showed that Stw 255 has a combination of features regarding the orientation of the posterior petrosal surface that may correspond to the external anatomy of KNM-WT 17000: an unflexed cranial base combined with a petrous axis that is relatively coronally oriented in the transverse plane. Fossils catalogued as Stw 255 may also be associated with the various specimens that make up Stw 252, but this is uncertain, as a second individual (Stw 265) of similar preservation was found in close proximity to Stw 252 (Lockwood and Tobias 2002:446-447, citations in original).

They go on to say they do not think that these specimens are sufficient evidence that another species was present, and they note details of a few other fragments that are different from the sample as a whole. They differ from Clarke (e.g. 1988), who would have divided the relatively complete cranial specimens into two samples.

Some other workers have suggested that individual specimens from Sterkfontein Member 4 might represent other species besides A. africanus. Kimbel and Rak (1993) proposed that Sts 19 probably represents Homo, and that the inclusion of the specimen into A. africanus inflates the variation within that species. This proposition was tested by Ahern (1998), who found the Sterkfontein Member 4 specimens to be quite variable without Sts 19 also. In other words, this site preserves a variable sample -- especially considering nonmetric traits observed on individual specimens.

The traits of Stw 183 and Stw 255 may fall in that category of variation, and Lockwood and Tobias (2002) suggest that possibility. I think the specimens are interesting because of whose traits they share. Studying A. africanus not as a branch of a cladogram, but as a real species with possible ancestors and descendants, the occasional presence of characters of earlier and later species is to be expected. The question is whether these characters document an ancestor-descendant relation for A. africanus and the robust taxa, or whether they might be shared by collateral taxa by virtue of common ancestry alone. The half-million years preceding the origins of Homo may have been just as interesting for the study of populations as the last half-million years.

References:

Ahern JCM. 1998. Underestimating intraspecific variation: the problem with excluding Sts 19 from Australopithecus africanus. Am J Phys Anthropol 105:461-480.

Clarke RJ. 1988. A new Australopithecus cranium from Sterkfontein and its bearing on the ancestry of Paranthropus. In (Grine FE, ed) Evolutionary history of the robust australopithecines. Aldine de Gruyter, New York. p. 285-292.

Kimbel WH and Rak Y. 1993. The importance of species taxa in paleoanthropology and an argument for the phylogenetic concept of the species category. In (Kimbel WH and Martin LB, eds) Species, species concepts, and primate evolution. Plenum Press, New York. p. 461-484.

Lockwood CA and Tobias PV. 2005. Morphology and affinities of new hominin cranial remains from Member 4 of the Sterkfontein Formation, Gauteng Province, South Africa. J Hum Evol 42:389-450.

On the Scientific American website, there is a long article by Michael Shermer (editor of Skeptic magazine), describing his trip to the World Summit of Evolution, held in the Galapagos Islands this month. Some of the attendees:

It was a veritable Who's Who of evolutionary theory, including William Calvin, Daniel Dennett, Niles Eldredge, Douglas Futuyma, Peter and Rosemary Grant, Antonio Lazcano, Lynn Margulis, William Provine, William Schopf, Frank Sulloway, Timothy White and others.

Shermer provides a rundown of many of the scientific presentations, and it is an interesting read. The paleoanthropology representative was Tim White, and Shermer gives him almost a whole page:

One of the best talks of the conference was delivered by the U.C. Berkeley paleoanthropologist Timothy White, in which he opened with a prediction made by Stephen Jay Gould in the late 1980s: "We know about three coexisting branches of the human bush. I will be surprised if twice as many more are not discovered before the end of the century." A glance at the extant fossil record looks like Gould was right. There are at least two dozen fossil species in six million years of hominid evolution. But the bush is not so bushy, says White. The problem lies in the difference between "lumpers" and "splitters" in species classification, and the social pressures to publish extraordinary new discoveries. If you want to get your fossil find published in Science or Nature, and you want the cover illustration, you cannot conclude that your fossil is yet another Australopithicus africanus [sic], for example. You better come up with an interpretation indicating that this new find you are revealing for the first time to the world is the most spectacular discovery of the last century and that it promises to overturn hominid phylogeny and send everyone back to the drawing board to reconfigure the human evolutionary tree. Training a more skeptical eye on many of these fossils, however, shows that many, if not most of these fossils belong in already well-established categories. White says that the specimen labeled Kenyanthropus platyops, for example, is very fragmented and is most likely just another Australopithicus africanus [sic]. "Name diversity does not equal biological diversity," White elucidated.

If I had a quote list, I'd add that one to it: "Name diversity does not equal biological diversity." On the other hand, White has himself had the cover of Nature once or twice....

And then there is this:

White then concluded his talk with a fascinating discussion of the recent discovery of fossil dwarf humans on Flores Island in the Malay Archipelago, located on the outside of Wallace's Line, meaning that even during the last ice age they could only have gotten there by boat. (White did note, however, that after last December's tsunami people were rescued from large floating rafts of natural debris, so it is possible that the founding population of Flores rafted there by accident and not design.) ... A second published specimen put to rest the pathology hypothesis that Homo floresensis was a microcephalic human. The best evidence, says White, points to insular dwarfing, a rapid punctuation event out of Homo sapiens that led to a shrinkage of these isolated people. Such dwarfing effects can be seen on this and other islands, where large mammals get smaller (like the dwarf elephant), and small reptiles get larger (like the Komodo Dragon). The chances of any living members of this species still existing in the hinterlands of Flores are extremely remote, but some observers have noted that the indigenous peoples of Flores recount a myth of small hairy humans who descend from the highlands to steal food and supplies.

You can read what I have to say about Homo floresiensis here. I'm telling you, the more this story gets repeated, the worse it's going to turn out.

Most of the meeting was relatively big-name evolutionary biologists of one kind or another. In the end, it sounds to me like the many of the invitees wanted to trash Darwinism to promote their own idiosyncratic theories. To some extent, Shermer displays his best skeptical take on these, although he describes one as "beyond [his] pay scale." A lot of famous scientists have problems with standard neo-Darwinism, and it seems that many were invited to this meeting, with very few representatives of the more standard point of view. So Shermer's article includes many "proclaiming the death of Darwin" stories. Interesting in this context that there appear to have been no evo-devo people at the conference, since this is probably the most important of the extensions to evolutionary theory, and one that resonates with pre-Darwinian biology to a much greater extent than ideas like Margulis' pansymbiosis or multilevel selection theory.

Read the article and see if you agree with Shermer that evolutionary biology is in a healthy state. My take is that a show of real health would have included a slightly different list of biologists.

Speaking of old papers, I was just re-reading this one from Duncan Baird and colleagues (2000).

What got me started was this line from the recent paper by Garrigan and colleagues (2005:3):

Aided by a novel experimental design, we present the first genetic evidence that statistically rejects the null hypothesis that our species descends from a single, historically panmictic population.

Of course, that didn't sound right to me, because people have been talking about evidence for archaic genes in recent humans for several years. The Baird study wasn't cited in that paper, and I returned to it to see what the evidence looked like. Here's the last line of the abstract (Baird et al. 2000:235):

To explain the presence of a few diverged haplotypes adjacent to the Xp/Yp and 12q telomeres, we propose a model that involves the hybridization of two archaic hominoid [sic] lineages ultimately giving rise to modern Homo sapiens.

This more detailed consideration of the problem of divergent haplotypes comes from the discussion:

Two alternative explanations for the presence of divergent haplotypes adjacent to two telomeres can be envisaged. First, the divergent haplotypes arose independently at separate subterminal loci within an archaic hominoid [sic] genome. The high level of exchange between subterminal repeat sequences then resulted in the relocation of one of the subterminal sequences with a telomere to the end of the same chromosome, thus creating two highly diverged haplotypes at one locus. We think, however, that this explanation is unlikely, since there is no evidence that "donor" loci exist in the modern genome. The results of linkage analysis indicate that the only copies of the sequences that can be amplified by the 12qA, 12qB, and 12qArev primers are linked to the end of 12q. Also, although a related copy of the 12q telomere-adjacent sequence is present on some copies of chromosomes 7q, the sequence in this location does not show more similarity to one 12q telomere-adjacent haplotype than to the other. In addition, there is no evidence that a second locus with homology to the Xp/Yp telomere-adjacent sequence is present in the human or in other great-ape genomes. It would therefore be necessary to assume that the "donor" loci for the ends of both chromosomes were present in an ancestral genome but have been lost from the modern human genome. Another explanation is that the diverged haplotypes arose, in separate archaic hominoid lineages, from a common ancestral sequence. These lineages would have to have been isolated for sufficient time to allow divergent haplotypes to arise as a result of sequential mutations and of fixation in each lineage for one predominant haplotype. The degree of sequence divergence between the haplotypes would be dependent on the mutation rates of the loci examined. The high mutation rate in the telomere-adjacent sequences would have resulted in rapid divergence of these sequences in the different lineages. A subsequent hybridization of two hominoid lineages would bring the highly diverged haplotypes together. The continued existence of the diverged haplotypes after the hybridization event would depend on factors such as recombination, drift, and founder effect, and it could vary between loci. This model implies that Homo sapiens may have evolved from a hybridization event between two hominoid [sic] lineages (Baird et al. 2000:247-248).

There's that "hominoid" again. Why hominoid instead of hominid? It turns out these polymorphisms are pretty ancient. Not hominoid-ancient, but, well, read for yourself:

Since the timing of the proposed hybridization event is unknown, it is not possible to suggest which hominoid lineages may have been involved; however, the common ancestor to the lineages must have existed >2 million years ago, perhaps coinciding with one of the Australopithecine species. Additional analysis of the 12q telomere and its adjacent sequence in other human populations may distinguish between the explanations outlined above, but it is not unreasonable to suggest that hybridization between lineages separated by 1.9 million years could occur, because the orangutan subspecies Pongo pygmaeus abelii and Pongo pygmaeus pygmaeus are capable of producing fertile offspring, despite the existence of molecular data that suggests that the two subspecies diverged 1.5 -- 1.7 million years ago (Zhi et al. 1996). Of the two diverged haplotypes in the orangutan Xp/Yp telomere-adjacent sequence (discussed above), one haplotype (orang-lower) was detected in both the orangutan subspecies, but the second haplotype (orang-upper) was detected only in the Pongo pygmaeus abelii subspecies (2/18 alleles) (Baird and Royle 1997; Baird, unpublished data). Furthermore, the observation of homoplasy in skeletons of the Australopithecine species A. africanus and A. afarensis suggests that human evolution was more complex than is currently understood (McHenry and Berger 1998a; McHenry and Berger 1998b), and, recently, a skeleton with both human and Neanderthal characteristics was identified (Duarte et al. 1999) (Baird et al. 2000:248).

So, definitely hominid, but fairly ancient: they place the divergence of the haplotypes at at least 1.9 million years. The story here is not the time depth alone, but the lack of intermediate haplotypes between two extremes; which is the same story offered by Garrigan et al. (2005). Of course, it's not the "archaic" part that they claim is new, it's the "statistical test" part. They're starting to sound like paleoanthropologists!

References:

Baird DM, Coleman J, Rosser ZH, Royle NJ. 2000. High levels of sequence polymorphism and linkage disequilbrium at the telomere of 12q: implications for telomere biology and human evolution. Am J Hum Genet 66:235-250. Full text online

Garrigan D, Mobasher Z, Kingan SB, Wilder JA, Hammer MF. 2005. Deep haplotype divergence and long-range linkeage disequilibrium at Xp21.1 provide evidence that humans descend from a structured ancestral population. Genetics (online before print).

Following up on an earlier post, Time Asia has a story on the Rampasasa "pygmies." After reading the article, my feeling is that paleoanthropology has, on balance, a negative effect on indigenous peoples. Take the following, for instance:

Some six generations of intermarriage with outsiders, says Rampasasa's headman Alfredus Ontas, have left few truly tiny individuals. But to prove their antecedents, he and other locals eagerly display photos of recently deceased relatives whom they say were of purer "short people" stock. "The brothers in this photograph were only 110 cm," Ontas says proudly, his broad smile revealing jagged teeth stained ox-blood red by betel nut. Another elder is introduced, who, as well as measuring only 135 cm tall, has a pelt of hair covering his arms and legs. "It was because we were so hairy that our ancestors hid in Liang Bua," says Jurubu. "They were embarrassed."

So either a "new paleoanthropological find" has already been incorporated into the ancestor myths of this village, or the people are already moving to capitalize on their newfound fame, or more likely both:

And the bones in the cave? "Of course, they were our ancestors," says Jurubu, with a touch of rheumy indignation. "They must have retreated into the cave after a hunt and got caught there when the river rose. Who else could it be?" That's proving to be a question for the ages.

But what stuns me about this article are the comments from Henry Gee, editor of Nature, which published the initial paper by Brown and colleagues (2004).

For Henry Gee, an editor at venerable Nature who was responsible for overseeing publication of the original H. floresiensis article, such squabbling is par for the course. "Science is a disputatious business, and human evolution is notorious for being even more disputatious. Historically, whenever anyone discovers a new hominid, a lot of people come along and say it's an ape or a diseased human." Gee, who says the critics haven't shaken his belief that a new species has been found, cites the example of another hotly debated discovery, that of Australopithecus africanus in 1924, the so-called "missing link" between apes and human ancestors. "Nature published that paper too and all the great and good in the scientific establishment refused to believe it." It took 25 years, but eventually the discovery was accepted, Gee says, noting that it will be a while before H. floresiensis achieves complete acceptance as well. "They're going to have to discover some more bones that prove this, but we have history on our side."

We have history on our side? I think I'll try that one next time I submit a paper to Nature: "Hey, I have history on my side, man. Those negative peer reviews? Dude, can't you see the 'great and good' are against me?"

To me, these sound like the comments of an advocate, rather than an editor who would be receptive to articles that refute the original interpretation. I hope that the quote was taken out of context. As it stands it certainly isn't helping Nature's standing as a "venerable" journal.

I am at the AAPA meeting in Milwaukee this week, and so posting is by necessity very light. However, the news of the new Sahelanthropus remains and CT reconstruction have come out this week. I have been thinking about them since I got a hold of the proofs last week, so I can post some comments about them. There are some thoughts I'm holding on to for now, however, since I have a manuscript that covers some of them. It's bad enough to be scooped by other people; I surely don't want to scoop myself!

BBC News story, with artist rendition from Nature cover.

The lead story seems to be the reconstruction, probably because it was intended to sort out many of the problems with the distortion in the original fossil. To some extent it succeeds in simplifying the interpretation. For example, the reconstruction clearly places the foramen magnum in a more anterior position than the original. It is not clear to me how the anatomy of the original could conform to the reconstructed base, but doubtless working with a CT is better than working with photographs.

Actually, the article does not place a great emphasis on the anterioposterior position of the foramen magnum. This is sensible, because chimpanzees and australopithecines overlap considerably in this position compared to other basicranial landmarks like the bicarotid line. TM 266 is within the region of overlap, both in the original distorted version and in the reconstructed version.

Instead, Zollikofer and colleagues make two complementary arguments for why the skull is hominid. The first concerns the angulation of the foramen magnum (characterized by the basion-opisthion line) compared to a line tangent to the upper and lower orbital margins.

Despite substantial differences in neck orientation, humans and non-human primates tend to locomote with their orbital planes (the line joining the superior and inferior margins of the orbits) approximately perpendicular to the ground. In addition, primates orient the upper cervical vertebrae approximately perpendicular to the plane of the foramen magnum, and with only a limited range (about 10 degrees) of flexion and extension possible at the cranio-cervical joint. The combined effect of these angular constraints is that the angle between the foramen magnum and the orbital plane is nearly perpendicular in Homo sapiens (103.2 +- 6.9 degrees, n = 23) but more acutely angled in Pan troglodytes (63.7 +- 6.2 degrees, n = 20), and other species with more pronograde postures. The foramen magnum angle relative to the orbital plane in the TM 266 reconstruction is 95 degrees, similar to that in humans and later bipedal hominids such as Australopithecus afarensis (AL 444-2) and A. africanus (Sts 5). TM 266-01-060-1 as a quadruped would requier an unusually extended angle of the neck relative to the plane of the foramen magnum (Zollikofer et al. 2005:757).

A weakness in this argument is that this angle is exquisitely sensitive to the reconstruction. That is, a small difference in the vertical position of either basion or opisthion (the front and rear points on the foramen magnum border, respectively) will have a large effect on the angle of the line passing through these points. But assuming the reconstruction is correct, it is fairly compelling evidence that the habitual posture of the head in Sahelanthropus was not like chimpanzees or gorillas.

The second argument concerns the downward lip of the nuchal crest, which they argue indicates the directionality of the nuchal muscles. It is true that some other hominids have a downward lip on this crest, but I would like to go through a large ape sample to see the range of variation in this trait. In any event, this feature cannot be isolated from the exceedingly unique nuchal morphology in this specimen; the orientation and function of the nuchal musculature cannot be assumed to be like that of other apes whether it had vertical posture or not.

So was it a biped? From the reconstruction alone it may not be possible to confirm or deny the hypothesis. A more vertical habitual posture might or might not imply facultative bipedality. One possibility that would not imply bipedality is that Sahelanthropus had long arms, on the scale of Dryopithecus or longer. In this case, a quadrupedal stance would involve a more vertical trunk position. The distinction between this adaptation and that of gibbons or dryopithecines would be the larger body size and consequent greater degree of terrestriality. This hypothesis might also explain other Miocene hominoids that have been suggested to be like bipeds in certain characters, including Ouranopithecus and Oreopithecus. A test of the relationship of trunk position, limb length, and cranial base morphology might be informative.

Setting aside the question of whether it was a biped, was it a hominid? These are different questions if we assume that the advent of hominid bipedalism followed after some significant time the divergence of hominids from chimpanzees. Aside from Sahelanthropus, the earliest comparably complete hominid cranial remains are less than half its age. The closest is the as-yet-undescribed StW 573 skull. Then is KNM-WT 40000, followed by the cranial remains from Hadar, including the AL 444-2 specimen. A. afarensis and later A. africanus both have extensive adaptations to masticatory force. The extensive nuchal plane of TM 266 is long, narrow, and flat, and it is unlike any early hominid. The browridges are larger (especially in proportion to its relatively small overall cranial size) than in any australopithecine. Thus, it is a challenge to explain exactly what this skull represents in adaptive terms. I think an explanation of its anatomy is in order before it is accepted as being phylogenetically close to the australopithecines.

The paper by Brunet et al. (2005) presents new mandibular and dental remains of Sahelanthropus, including a lower canine with apical wear.

The new material presented here is important for several reasons. . . . The S. tchadensis hypodigm now includes a minimum of six individuals (a maximum of nine) from three sites in a small area of the Anthracotheriid Unit. Second, these new fossils now present a more complete and reliable understanding of this earliest known hominid taxon. S. tchadensis shares major derived features with other recognized hominids that are consistent with its position in the hominid clade, close to the last common ancestor of chimpanzees and humans. In the dentition these anatomical characters are a non-honing C/P₃ complex; no diastema between C and P₃; a vertical symphysis with weak transverse tori; canines with a small crown and long root; a lower canine crown with a large distal tubercle, both shoulders being very low; an upper P³ with a steeply sloping buccal surface; postcanine teeth with maximum radial enamel thickness intermediate between chimpanzees and australopithecines; and bulbous, slightly crenulated postcanine occlusal morphology. All the hominid mandubular premolar specimens from Toros-Menalla have the same root pattern, with two roots and three separate pulp canales in each premolar (one mesial and two distal) retaining the presumed primitive condition for the Pan/Homo clade (Brunet et al. 2005: 754).

This is a bit of a confused list, since very few of these characters are actually both derived and shared with later hominids. For example, a character that retains "the presumed primitive condition for the Pan/Homo clade" clearly is not a "major derived feature" shared with "other recognized hominids."

The most persuasive similarity with hominids is the reduced canine. But to my eyes, the Sahelanthropus lower canine is distinct from later hominids, especially considering the prominent ridge, or shoulder, around the base of the crown. This feature is found among dryopithecines, and it may simply be a primitive feature retained in an otherwise reduced canine. So the idea that this is intermediate between a larger, ape-like canine and the canines of later hominids is possible, but not demonstrated.

So in my view, the hypothesis that Sahelanthropus is in fact an early hominid has not been strongly substantiated. In many of its features it is basically plesiomorphic, and shares the morphology of a number of Miocene apes. In a few features, it shares a derived (or partially derived) morphology with australopithecines. It also has cranial features such as its long flat nuchal torus and hulking browridge that are derived, not shared with later hominids, and would therefore tend to indicate a separate evolution for this taxon. In my opinion, we probably have entered a time period early enough that the relationships of early hominids, early chimpanzees, gorillas and their ancestors may not be readily resolved with morphological comparisons.

References:

Brunet M et al. 2005. New material of the earliest hominid from the Upper Miocene of Chad. Nature 434:752-755.

Zollikofer CPE et al. 2005. Virtual cranial reconstruction of Sahelanthropus tchadensis. Nature 434:755-759.

Wood and Lieberman (2002) attempt to systematize the variation in fossil A. boisei. Their hypothesis is that some kinds of craniodental variables may be expected to be more variable than others, by virtue of their function. In particular, they consider it likely that variables that reflect high magnitudes of mechanical strain during life will be more variable than those that reflect low magnitudes of strain. The strain connection is based on the notion that phenotypic plasticity may be a significant contributor to the phenotypic variance of traits, and especially for areas of the skull or dentition that are affected by strain during life. This hypothesis is predicated on the notion that the effects of such forces during life are actually variable, rather than constantly presenting the same degree of strain in different individuals. There is no discussion of this issue, because the empirical data ultimately support the connection. The areas of the skull under masticatory strain are more variable than other regions.

It is not clear exactly what accounts for this observation. For example, one hypothesis would be that the masticatory regions show a higher degree of sexual dimorphism than other parts of the skull. Another might be that there is ontogenetic variation between older and younger adults in these characters, and both are represented in the sample. Neither of these hypotheses nor others can be tested with the data presented.

But the causes of the variability are not necessarily relevant to the paper's conclusions about taxonomic problems. Most notably, they conclude that features related to masticatory strain are not well suited to testing taxonomic hypotheses in fossil species. Instead, they recommend basing judgments about species on features that are typically less variable in living analogues.

I think this conclusion is generally right, and it would be interesting to see the consequences of following it through (for example, as applied to earlier hominids). For example, would there be any disagreement about the status of A. africanus if this criterion were followed?

On the other hand, who is to say that a fossil species must resemble the pattern of variability of (essentially) four living species of hominoids? Would we be confortable applying this criterion to Dryopithecus? Proconsul?

The paper appears to present the strain story as a stopgap between splitting and lumping. The fossil instance at stake is the addition of remains from Konso to A. boisei. Wood and Lieberman conclude that the Konso A. boisei specimens do not markedly extend the range of variation in fossil A. boisei. In this, they appear to be picking an argument with Gen Suwa and colleagues (1997), who argued that the Konso specimens were different in many respects from earlier A. boisei. That paper wanted to make the argument that most hominid species may have had as-yet-unrecognized variability; this one wants to argue that most of the as-yet-unrecognized variability probably isn't taxonomically interesting. A minor point, but one that illustrates the predispositions of the authors in each case.

Interestingly, the paper also tests the notion that dental features should be less variable than skeletal features because dental features exhibit higher heritability. They find that although dental measurements do tend to be slightly less variable in the observed data, there is no significance to the relation. In other words, traits that are more heritable are not less variable within species in these data.

References

Wood BA and Lieberman DE. 2002. Craniodental variation in Paranthropus boisei: a developmental and functional perspective. Am J Phys Anthropol 116:13-25.

Tanya M. Smith and colleagues (2003) measured the enamel of two Afropithecus molars, examining both their thickness and the periodicity of enamel formation. This was of interest because Afropithecus was thought to be the earliest thick-enameled ape.

Enamel thickness

Enamel thickness is not a simple value. The morphology of the tooth crowns are convoluted, and the enamel varies in thickness across the crown. Likewise, larger teeth might be expected to have thicker enamel than smaller teeth, just because of their size. A full study of the thickness of the enamel involves sectioning the tooth and taking observations of the area of the section taken up by enamel. In this study, relative enamel thickness was assessed as follows:

Relative enamel thickness was calculated by dividing the area of the enamel cap by the length of the enamel dentine junction, and this quantity was then divided by the square root of the area of the dentine and finally multiplied by 100. This provides a dimensionless index of enamel thickness that is suitable for comparisons across taxa (287).

In other words, enamel area (a square measure) is divided by the length of the enamel junction (a linear measure corresponding to the tooth topography and tooth size) and the square root of the dentine area defined under the enamel cap (a linear measure corresponding to the tooth size minus enamel). This isn't the only way one might measure relative enamel thickness, but scaling is inevitably a problem in structures with complex shapes.

The results list Afropithecus along with a number of other hominoids (which is why I found the paper). I reproduce the data here from the table on page 291, adding the value estimated for Gigantopithecus by Dean and Schrenk (2003):

Taxon	RET	Range	Category
Proconsul africanus	8.5		thin
Gorilla gorilla	10.0	6.8 -- 13.4	thin
Pan troglodytes	10.1	7.0 -- 13.3	thin
Hylobates lar	11.0		thin
Dryopithecus laietanus	12.7		intermediate thin
Oreopithecus bambolii	13.0		intermediate thin
Pan paniscus	13.6		intermediate thin
Proconsul major	13.7		intermediate thin
Lufengpithecus hudeniensis	14.1		intermediate thin
Rangwapithecus gordoni	14.9		intermediate thick
Pongo pygmaeus	15.9	11.3 -- 20.5	intermediate thick
Proconsul heseloni	17.0		intermediate thick
Sivapithecus sivalensis	19.2	16.3 -- 20.9	thick
Griphopithecus sp.	19.3	16.5 -- 23.0	thick
Afropithecus turkanensis	21.4	19.9 -- 22.9	thick
Australopithecus africanus	21.4	21.3 -- 21.6	thick
Homo sapiens	22.4	13.8 -- 32.3	thick
Proconsul nyanzae	22.4		thick
Gigantopithecus blacki	23		thick
Lufengpithecus lufengensis	24.1		thick
Gracopithecus freybergi	25.9		thick
Paranthropus robustus	29.6		thick

The RET is relative enamel thickness, and the ranges given vary in sample sizes. Looking over the extant species, it is clear that the ranges of relative enamel thickness are pretty great. It is not clear from this tabulation if there are any patterns -- for example, if enamel thickness was relatively constant but tooth size varied, that would create some variation in relative enamel thickness. In any event, the small differences among many of the fossil species probably do not signify significant differences. Perhaps the broad categories of thin, thick and intermediate are the best one can do for the fossils.

Development rate

The enamel in teeth is secreted during development by cells called ameloblasts. The ameloblasts begin at the enamel-dentine junction and migrate outward toward the eventual crown surface. The completed enamel has a prismatic crystal structure, with prisms oriented more or less perpendicularly from the enamel-dentine junction. The ameloblasts alternately speed and slow down enamel deposition in accordance with circadian and other cyclic processes. This cyclicity results in undulations of the enamel prisms as they radiate toward the tooth surface (described further in Aiello and Dean 1990). The cyclicity also causes visible striations in the enamel that are visible in cross section.

One type of striation is generated by the growing field of ameloblasts at approximately weekly intervals. These are called striae of Retzius, and each one represents the external enamel surface at a one stage of crown development. The striae of Retzius on the sides of the tooth intersect with the enamel surface, forming raised lines called perikymata Between the striae of Retzius are a series of smaller cross striations that represent daily enamel deposition along hte enamel prisms. The number of these between each pair of Retzius lines is referred to as the periodicity of the enamel development. Together, the periodicity and the count of striae of Retzius allow an estimate of the time of enamel formation, which may be informative about the developmental rate of the teeth.

The estimates for enamel formation time in Afropithecus from tooth sections indicate a time of between 2.43 and 3.10 years (Smith et al. 2003:293). According to the study, this is similar to crown formation times in living hominoids. In the abstract, they put the conclusion as:

Although thick enamel may be formed through several developmental pathways, most Miocene hominoids and fossil hominids with relatively thick enamel are characterized by a relatively long period of cuspal enamel formation and a rapid rate of enamel secretion throughout the whole cusp, but a shorter total crown formation time than thinner-enameled extant apes. (283)

More on Afropithecus

More on fossil apes

References:

Aiello L and Dean C. 1990. An Introduction to Human Evolutionary Anatomy. Academic Press, Oxford, UK.

Dean MC and Schrenk F. 2003. Enamel thickness and development in a third permanent molar of Gigantopithecus blacki. J Hum Evol 45:381-387.

Smith TM, Martin LB, and Leakey MG. 2003. Enamel thickness, microstructure and development in Afropithecus turkanensis. J Hum Evol 44:283-306.

A recent spate of articles has carried on a debate about the age of the Sterkfontein hominids. Sterkfontein is a complicated site, including several distinct caverns and deposition layers, called members. The dating of these layers is a serious problem because of their complex stratigraphy and the lack of volcanics that could be subjected to radiometric dating. Until recently the only insights into the age of the fossils came from uranium-series dating and paleomagnetic analysis of calcite deposits in the caves.

The Sterkfontein deposits are divided into six members, and hominid have been recovered from Member 5, Member 4, and Member 2. Most of the hominid remains assigned to Australopithecus africanus come from Member 4, which was long thought to date to between 2.8 million and 2.6 million years. Before Member 5 was deposited, there was erosion on the top of Member 4, and the two are separated by an unknown period of time. This deposit is generally thought to be less than 2 million years in age, perhaps extending as recently as 1.4 million years (Kuman and Clarke 2000). In recent years, excavations lower in the deposit, including the Jacovec cavern and the Silberberg grotto, have produced hominid fossils attributable to Member 2. These were initially believed to be around 3.5 million years old.

The most important fossils from Member 2 belong to the specimen StW 573. The foot bones of this skeleton were initially found in a dump of breccia outside the cave (Clarke and Tobias 1995). The origin of the bones was traced to Member 2, and they were matched to the broken end of a tibia still in situ in the Silberberg grotto. The skeleton is now known to be largely complete, including a skull and mandible, forelimb and hindlimb elements, and much else. It appears to be considerably more complete than the "Lucy" skeleton from Hadar, AL 288-1, or any other australopithecine, but it is not yet fully excavated from the overlying breccia and flowstone. The idea that this skeleton might date to 3.5 million years was potentially very important. At this date, it would be a contemporary of A. afarensis from Laetoli and Maka (it would be earlier than the Hadar deposits). It is not clear yet whether StW 573 anatomically resembles A. afarensis or is more similar to later South African hominids, but this would certainly be an important question to answer from the respect of early hominid phylogeny.

Making Sterkfontein later

McKee (1996) suggested that Member 2 was likely immediately earlier than Member 4. His argument was that the fauna of Member 2 were all found in Member 4, but several species were absent from Makapansgat Member 3 and 4, which date to between 3.2 and 2.9 million years. He proposed that this could be explained by the chance lack of these species at Makapansgat, but viewed that possibility as less likely than the hypothesis that the species appeared after Makapansgat Member 4, to be found in the later Sterkfontein deposits.

Clarke and Tobias (1996) responded to this argument by noting the long stratigraphy of Member 3 between the Member 2 and 4 sequences, with several flowstones that must have taken a long time to deposit. They note that although Makapansgat does not preserve all the Member 2 fauna, the species that are absent are known from other African sites prior to 3.5 million years, and therefore are not of use in dating the deposits. The exception is one baboon species, Papio izodi, which is known only from Member 4 and Taung, and may therefore be rare enough to be absent from other sites.

Berger and colleagues (2002) argued that the entire Sterkfontein sequence is substantially later than had previously been thought. They base their argument on biostratigraphic and paleomagnetic considerations. They have a number of reasons for this:

1. The presence of Equus in the deposit, which is not radiometrically dated in Africa earlier than 2.36 million years ago.
2. In addition to Equus, several other taxa are found in Member 4 that do not have secure radiometric dates above 2.5 million years anywhere in Africa.
3. A later date for Member 4 would suggest that the sequence of magnetic samples from the site should be displaced earlier by a reversal cycle. This would place the top of Member 2 within the Olduvai subchron, and the StW 573 hominid would then date to between 2.15 and 3.04 million years ago. If this is displaced by another cycle more recently, StW 573 would date to as recently as 1.07 to 1.95 million years.

As far as Equus, Kuman and Clarke (2000) are at pains to show that it actually may not occur in Member 4. According to them, only one equine tooth has been excavated from Member 4 in situ, with the remaining bones taken from fill that may derive from Member 5. They argue that the one tooth is insufficient evidence of the presence of the genus, considering the possibility of erosion from later deposits.

Making Sterkfontein earlier

Partridge and colleagues (2003) dated the Sterkfontein Member 2 deposits by using the radioactive decay of cosmogenic isotopes. These are created when cosmic rays from outer space interact with the elements in quartz grains near the earth's surface. In particular, aluminum-26 and beryllium-10 accumulate in quartz grains at a predictable ratio. These two isotopes have different half-lifes (²⁶Al = 1.02 million years, ¹⁰Be = 1.93 million years), which means that once the quartz grain is buried and no longer exposed to cosmic rays, the ratio of the two isotopes changes.

Sediments near the StW 573 specimen gave a date estimate of 4.17 million years, while the orange breccia in the Jacovec Cavern gave an estimate of around 4.02 million years. These date estimates are substantially earlier than were previously estimated for these localities at the site.

It was not possible to date Member 4 in this way, because it is shallow enough that cosmic rays can still affect the quartz grains used for dating.

Partridge et al. (2003) do not present a response to Berger et al. (2002), except to note that their earlier dating "is unsustainable on stratigraphic and faunal as well as on paleomagnetic grounds" (612, note 12). In any event, there seems to be no strong biostratigraphic reason to place Member 2 at either an earlier or later date; the preserved fauna is not specific as to age.

Member 5 stratigraphy

Kuman and Clarke (2000) review the stratigraphy of Member 5. The most important hominid specimen that has been attributed to Member 5 is StW 53, a nearly complete skull that has been variably attributed to A. africanus or Homo habilis. Kuman and Clarke (2000) show that the skull derives from an area that likely is intermediate in age between Members 4 and 5 proper. They call this area the "StW 53 Infill." No artifacts derive from this area. The authors argue that the infill is likely more recent than Member 4 because of the presence in the deposit of Theropithecus oswaldi, a species found in the later Swartkrans Members 1--3, and associated with drier open grassland habitats. On this basis, they place the StW 53 Infill between 2 million years ago and 2.4 million years, which marks the earliest appearance of T. oswaldi in East Africa.

According to Kuman and Clarke (2000), Member 5 can be divided by the presence of two distinct tool industries. The Oldowan Infill dates to between around 2 million and 1.7 million years ago, and preserves 3245 excavated artifacts (Field 1999). The paleoenvironment seems to indicate a grassland. The later phase is referred to the Acheulean because of the presence of bifaces, and is placed between 1.7 and 1.4 million years ago. Like the earlier Oldowan infill, the Acheulean infill represents a predominantly grassland fauna, similar to Swartkrans.

Kuman and Clarke (2000) provide a list of hominid fossils with their probable associations in the stratigraphy. They also discuss the taxonomy of the fossils and their resemblances with elements of the earlier Member 4 and Swartkrans remains.

More on Sterkfontein

More on Makapansgat

References:

Berger LR, Lacruz R, de Ruiter DJ. 2002. Brief communication: Revised age estimates of Australopithecus-bearing deposits at Sterkfontein, South Africa. Am J Phys Anthropol 119:192-197.

Clarke RJ, Tobias PV. 1995. Sterkfontein Member 2 foot bones of the oldest South African hominid. Science 269:521-524.

Clarke RJ, Tobias PV. 1996. Faunal evidence and Sterkfontein Member 2 foot bones of early hominid. Science 271:1301-1302.

Field AS. 1999. An analytic and comparative study of the Earlier Stone Age archaeology of the Sterkfontein Valley. MasterÕs thesis, University of the Witswatersrand.

Kuman K, Clarke RJ. 2000. Stratigraphy, artefact industries and hominid associations for Sterkfontein Member 5. J Hum Evol 38:827-847.

McKee JK. 1996. Faunal evidence and Sterkfontein Member 2 foot bones of early hominid. Science 271:1301.

Partridge TC, Granger DE, Caffee MW, Clarke RJ. 2003. Lower Pliocene hominid remains from Sterkfontein. Science 300:607-612.

Pickering and colleagues (2004) examine the fauna from Sterkfontein Member 2, coming to the following conclusion:

In summary, the mammalian fauna from Member 2 indicates a paleohabitat that was probably typified by rolling, rock-littered and brush- and scrub-covered hills (suitable for caracals and Makapania, and also commonly exploited by papionins). The valley bottom might have retained standing water year-round, and perhaps supported a tree line or restricted riverine forest, fringed by open woodland or grassland -- a setting appropriate for Alcelaphini, the abundant monkeys, and ambush predators, such as leopards (292).

The authors find this paleoenvironmental reconstruction to be basically similar to other contemporary hominid sites, such as Kanapoi (Wynn 2000), as well as the fauna from the Jacovec cavern. All of these contrast with earlier hominid sites, which were predominantly closed woodlands (WoldeGabriel et al. 2001; Pickford and Senut 2001). Indeed, WoldeGabriel and colleagues (2001:177) conclude that:

The demonstration that the earliest hominids consistently derive from strata bearing indicators of wooded environments may explain their rarity at some sites. It therefore seems increasingly likely that early hominids did not frequent open habitats until after 4.4 Myr. Before that, they may have been confined to woodland and forest habitats.

The final conclusion of Pickering and colleagues (2004) is about the relative abundance of hominid fossils, which are much rarer in the overall composition of the fauna than at sites like Kanapoi. They consider that this relative absence of hominids may either result from a relative scarcity of hominids in the environment, or instead from taphonomic biases that may have led hominids to be underrepresented in Member 2 in particular. They point out that the Member 2 hominids are relatively unaffected by carnivores, with an absence of toothmarks or other indicators of predation. This contrasts with the hominid fossils from the open-air sites in East Africa, where marks from carnivores and other predators are common In their view, the hominids mainly got into the deposit by walking in and dying. This is not as common as carnivores carrying in prey to eat it, but both recent papionins and hominids are known to enter caves -- in the case of the baboons, apparently because caves are cool places to escape the sun. They do not evaluate whether predation may have been higher in Member 4, but are apparently open to the possibility that differences in the taphonomy are mainly consequences of differences in hominid behavior.

More on Sterkfontein

More on A. africanus

References:

Barrett L, Gaynor D, Rendall D, Mitchell D, Henzi SP. 2004. Habitual cave use and thermoregulation in chacma baboons (Papio hamadryas ursinus). J Hum Evol 46:215-222.

Leakey MG, Feibel CS, McDougall I, Ward C, Walker A. 1998. New specimens and confirmation of an early age for Australopithecus anamensis. Nature 393:62-66.

Pickering TR, Clarke RJ, Heaton JL. 2004. The context of Stw 573, an early hominid skull and skeleton from Sterkfontein Member 2: Taphonomy and paleoenvironment. J Hum Evol 46:279-297.

Pickford M, Senut B. 2001. The geological and faunal context of Late Miocene hominid remains from Lukeino, Kenya. C R Acad Sci Paris Sciences de la Terre et des planetes 332:145-152.

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

WoldeGabriel G, Haile-Selassie Y, Renne PR, Hart WK, Ambrose SH, Asfaw B, Heisken G, White TD. 2001. Geology and paleontology of the late Miocene Middle Awash Valley, Afar Rift, Ethiopia. Nature 412:175-178.

Wynn JG. 2000. Paleosols, stable carbon isotopes, and paleoenvironmental interpretation of Kanapoi, northern Kenya. J Hum Evol 39:411-432.

The chemical analysis of bones to interpret diet rests on the observation that different foods vary in the composition of different chemical elements or isotopes. Isotopes are different forms of an element that have different numbers of neutrons in their atomic nuclei (if they had different numbers of protons, they would be different elements). The number of neutrons in the nucleus affects the atomic weight of the isotope, and for this reason different isotopes may be taken up differently by different kinds of plants or animals, or they may be more or less abundant from different natural sources, such as the different mineral compositions of local soils. The chemical composition of an animal depends on the foods that it has eaten over the course of its life. Therefore, different kinds of animals may have different chemical signatures based on their preferred diets. If these isotopes are stable, then they may be preserved in fossil remains long after the death of the individual, and paleontologists may be able to access these ratios and make interpretations about the diets of ancient species. The amount of preserved material varies depending on the type of tissue examined, so that chemical analyses are usually expressed in terms of the ratio or proportion of one isotope or element to another. The major stable isotopes that have been examined in fossil hominid remains include the ratio of strontium (Sr) to calcium (Ca) and the ratio of carbon-13 (¹³C) to carbon-12 (¹²C).

Strontium/calcium ratios

Strontium and calcium are chemically similar elements that occupy the same column on the periodic table. For this reason, strontium can be taken up by plants in the place of calcium, and the two form a ratio that depends on the environmental abundance of strontium. When herbivores eat the plants, their bodies preferentially incorporate calcium instead of strontium, so that their Sr/Ca ratio is lower than that of the plants. And when carnivores eat the herbivores, they again incorporate more calcium than strontium, so that their Sr/Ca ratio is lower than the herbivores. Taken together, this means that we could infer the general diet composition (trophic level) of a fossil hominid if we knew its ratio of strontium to calcium. This wouldn't tell everything about the diet, and in fact it leaves many blanks. But with respect to the question of whether early humans were significant meat eaters, and whether robust australopithecines and other early hominids significantly differed in diet, this technique has great potential to inform.

One thing that is worth noting about these kinds of chemical ratios is that they reflect the average diet of ancient hominids across a large part of their lifespan. This time probably varies with circumstances, but it must always have included multiple years of dietary intake. This means that these ratios may respond to different aspects of the diet than the anatomy and size of the teeth, especially if the teeth were significantly adapted to fallback foods that did not make up the majority of the dietary intake of the animal.

Analysis of strontium and calcium in fossil bones requires some background work. The amount of strontium available to the food web depends on the local soil composition, so the Sr/Ca ratio may vary among samples of the same kind of animal taken at different sites. This means that different kinds of herbivores, carnivores, and omnivores must be sampled at the same location in order to interpret their Sr/Ca ratios. Additionally, it appears that fossil bone and fossil teeth may vary in their preservation of Sr/Ca ratios. The initial work on early hominid Sr/Ca ratios was done by Andy Sillen (1992) on fossil bone from Swartkrans. But Sillen and others have shown that the process of fossilization alters composition of bones in ways that may skew or erase the endogenous ratio of strontium to calcium.

Sponheimer and colleagues (2005b) examine the ratio of strontium to calcium in the tooth enamel of fossil hominids from South African sites. Enamel is less susceptible to diagenesis (change over time) than bone, and should preserve more accurate estimates of Sr/Ca ratios. A possible issue is that enamel is mainly deposited early in life, and therefore reflects preweaning or early juvenile diets that may not be fully representative of the dietary repertoire of the animal. To examine this, Sponheimer et al. examined comparative samples of mammals from the fossil localities and from recent contexts, finding that the Sr/Ca ratios did differentiate browsers, grazers, and carnivores from each other. The differences between these animal groups are that the grazers have the highest Sr/Ca ratios, and the carnivores and browsers. Browsers eat a high proportion of leafy species that tend to have lower Sr/Ca ratios, and as a consequence their Sr/Ca ratios tend to be slightly lower than those of the carnivores.

The analysis found that the remains of A. africanus from Sterkfontein Member 4 had relatively high Sr/Ca ratios, easily within the range of or even exceeding those of the grazers. A. robustus from Swartkrans Member 1 had substantially lower Sr/Ca ratios than A. africanus, but these were within the range of all the other animals, including browsers, grazers, and carnivores.

Sponheimer and colleagues (2005b) note that the results here were different from those of Sillen (1992), who showed the robust australopithecine bones to have rather low Sr/Ca ratios. Sillen suggested that this meant that the robust australopithecines was significantly omnivorous. The tooth enamel is consistent with a broad range of diets, so it does not disprove the hypothesis that robust australopithecines were omnivores, but it does not specifically disprove the notion that they were exclusive herbivores either.

The bottom line is that it is very difficult to differentiate diets with this kind of information. One problem is the nature of the overlap among the comparison samples. The whisker plots overlap substantially among these, and since they show the 10th and 90th percentiles, the extent of overlap may have been almost complete. This is not to say that the distributions are the same, but that individual fossils that are in the area of overlap (which would include most of the robust specimens and many of the A. africanus specimens) may not be diagnosed. Fortunately the study included a large number of teeth, so that samples may be compared to each other, and these samples are significantly different from each other. Assuming that the teeth have been assigned correctly to samples, this provides some confidence in the idea of a dietary difference between these samples.

A more important problem is that very different dietary compositions may have the same Sr/Ca signature. For example, a leaf browser that included some grass seeds in its diet might have the same Sr/Ca ratio as a fruit eater that included significant meat. And the Sr/Ca ratio does not give any indication of seasonal variations that might have ecological importance.

Carbon stable isotopes

Not all plants photosynthesize in the same way. The majority of plant species use a three carbon photosynthetic pathway. These are called C₃ plants. But some plants use instead a four carbon pathway, and these are called C₄ plants. The C₄ plants are a minority, but include a large proportion of grasses and sedges, and a few other kinds of plants.

There are two stable isotopes of carbon in nature. Most of this carbon has six neutrons, resulting in an atomic weight of 12. But a minority of carbon has seven neutrons, with an atomic weight of 13 (an additional small proportion is the radioactive carbon 14). The C₃ photosynthetic pathway preferentially includes carbon 12 (¹²C), so that C₃ plants have a ratio of ¹³C to ¹²C that is substantially lower than the ¹³C/¹²C ratio in nature. For C₄ plants, this discrimination is not as great, so that C₃ plants and C₄ plants differ in their ¹³C/¹²C ratios. Animals obtain their carbon from the foods they eat, so that the ¹³C/¹²C ratio of a herbivore marks the proportion of C₃ and C₄ plants in its diet. Likewise, the ¹³C/¹²C ratio of a carnivore reflects the plant diets of its prey species.

For example, grazers tend to eat a high proportion of grasses, which in Africa are predominantly C₄ plants. This means that grazers have a relatively high ¹³C/¹²C ratio compared to other herbivores. It also means that carnivores who focus on grazers as prey species also have a high ¹³C/¹²C ratio. As noted by Sponheimer et al. (2005a:302): "the tissues of zebra, which eat C₄ grass, are more enriched in ¹³C than the tissues of giraffe, which eat leaves from C₃ trees."

A number of studies have examined the ¹³C/¹²C ratio in early hominid remains, focusing on those from the South African caves (Lee-Thorp et al. 1994; Sponheimer and Lee-Thorp 1999; van der Merwe et al. 2003). These studies are reviewed along with new results by Sponheimer and colleagues (2005a). The two basic results are that A. africanus and A. robustus are indistinguishable from their ¹³C/¹²C ratios, and that both australopithecine species have ¹³C/¹²C ratios that are elevated compared to C₃ consumers and intermediate between them and C₄ grazers. The fact that their ratios are lower than C₄ grazers is not surprising, since australopithecines clearly did not eat grass. But if they depended largely on fruits, nuts, or other C₃ foods, then it is difficult to explain why they should have stable isotope ratios that reflect a partial consumption of C₄ foods.

Several hypotheses might explain this observation:

1. Australopithecines may have eaten underground storage organs of C₄ plants, such as grass corms or tubers of certain sedges.
2. They may have eaten seeds from C₄ grasses.
3. They may have eaten the meat from grazing species.
4. They may have eaten termites that relied on grasses and other C₄ species.
5. Diagenesis of ¹³C/¹²C ratios in fossils may have altered the isotopic signature, which actually may have been the same as that of C₃ consumers (Schoeninger et al. 2001).

Sponheimer and colleagues (2005a) address the last hypothesis by testing a greater number of australopithecine teeth, finding results consistent with earlier findings. It is not obvious that this eliminates doubt entirely, but more samples provide more confidence that a real phenomenon has been observed. A comparison of all the hominids with recent C₃ consumers shows clearly that they are significantly different, with relatively little overlap. They are also very different from the fossil C₃ consumers preserved at the same sites (Sterkfontein and Swartkrans), which include browsing antelopes and giraffids. They are also distinct from C₄ grazers in having a lower ¹³C level. From these values, Sponheimer and colleagues (2005a:305, emphasis in original) write:

[T]he data suggest that Australopithecus and Paranthropus ate about 40% and 35% C₄-derived foods respectively. Such a significant C₄ contribution, whatever its origin, is very distinct from what has been observed for modern chimpanzees (Pan troglodytes). Schoeninger et al. (1999) found no evidence of C₄ foods in chimpanzee diets even in open environments with abundant C₄-grass cover.

With respect to the termites and sedges, Sponheimer and colleauges (2005a) found that termites in open environments do have a high C₄ proportion, while South African sedge species were found to be predominantly C₃ plants. This means that termites might have provided part of the C₄ component of early hominid diets, but the underground storage organs of sedges most likely did not. This does not mean that hominids may not have used sedges as a resource, but instead that such use would not explain their relatively high C₄ proportion. And a diet of 35 to 40 percent termites seems quite high, so even if these were included in the diet, there were likely other C₄ sources for the early hominids.

Another factor of the observations is that A. africanus teeth were quite variable in their ¹³C levels. Sponheimer and colleagues (2005a) suggest that one hypothesis to explain this variability would be if the sample changed over time--for example, in response to environmental change toward more open environments. Such changes in environment may be evidenced by a difference in the stable oxygen isotope ratios of the Sterkfontein and Swartkrans hominids. But when the ages of fossils were compared to ¹³C/¹²C ratios, there was no change over time, indicating that whatever dietary changes may have occurred, they evidently did not greatly affect the C₄ proportion in the diets of the australopithecines. Sponheimer and colleagues (2005a:308) conclude that the australopithecines with high variability may simply have been "extremely opportunistic primates with wide habitat tolerances that always inhabited a similarly wide range of microhabitats regardless of broad-scale environmental flux."

Combining the data

Can these different sources of evidence be put together into a single picture of ancient hominid diets? The answer is yes, but unfortunately there is more than one hypothesis that may fit the bill. The facts that must be explained are as follows:

1. High Sr/Ca ratios in A. africanus
2. Moderate Sr/Ca ratios in A. robustus
3. High proportion of C₄ sources in both A. africanus and A. robustus
4. Dental anatomy unsuited to leaf or grass eating in either species
5. Tooth wear and anatomy reflecting hard, brittle food consumption by robust australopithecines (Grine 1986; Grine and Kay 1988), and possibly similar but to a lesser degree in other early hominids (Ungar 2004).

Sponheimer et al. (2005b) treat the first of these observations as the most problematic, and try to account for it with hypotheses that are consistent with the other observations. One hypothesis is that early hominids were insectivorous. They indicate that modern insectivores do have higher Sr/Ca ratios than other faunivores (153). In combination with possible evidence for termite digging at Swartkrans (Backwell and d'Errico 2001), this observation might suggest that early hominids used termites and other insects as a significant food source, even moreso than living chimpanzees. Sponheimer and colleagues judge this hypothesis as problematic because the fossil hominids differ from recent insectivores in having a low ratio of barium to calcium (154). One may also add that the robust australopithecines from Swartkrans did not have especially high Sr/Ca ratios, while there has not yet been evidence of termite digging for earlier hominids.

A second hypothesis is described as follows:

We have noticed that among the modern fauna that have the unusual combination of high Sr/Ca and low Ba/Ca are warthogs (Phacochoerus africanus) and mole rats (Cryptomys hottentotus (Sponheimer, unpublished data), both of which eat diets rich in underground resources such as roots and rhizomes. Thus, the possibility of greater exploitation of underground resources by Australopithecus compared to Paranthropus requires consideration. In addition, the slightly enriched Sr/Ca of Paranthropus compared to papionins might also be evidence of increased utilization of underground resources.

This last point about A. robustus may be reaching. On the other hand, this leaves the dietary mix issue somewhat unsettled. For example, what if both A. africanus and A. robustus ate underground resources, but A. robustus also ate meat? Or if A. africanus also ate insects. And so on. It seems unclear that anything short of a clear identity of diet between an early hominid and a modern analog in the African fauna will leave the possibility of exotic mixes.

This leaves us to reflect on the full pattern of evidence more closely. How is the hard, brittle diet inferred from dental anatomy and wear reconcilable with the hypothesis that australopithecines were eating the tough, fibrous underground storage organs of C₄ plants?

Peters and Vogel (2005) address the issue of C₄ diet proportion by examining the range of C₄ plants that may have been available to early hominids. They make a number of observations:

1. C₄ sedges that produce edible roots, tubers, or stems are water-reliant, and do not compete with grasses in areas where drought occurs seasonally. They are therefore limited to relatively permanent watercourses including areas that are seasonally inundated with water. The South African sites do not represent such wetlands.
2. Interestingly, C₄ grasses have an evolutionary origin in the late Middle Miocene, and had increased in abundance in the African flora by the origin of the hominids.
3. A majority C₄ food intake by early hominids seems unlikely because of the wide availability of hominid-edible C₃ foods in areas where the relatively rarer C₄ hominid-edible plants also exist.
4. Mature tubers of C₄ sedges appear to have toxicity that may have impeded their edibility by early hominids, and they could probably have been consumed only in very small amounts.
5. A number of potential animals may have provided a C₄ component for early hominids, beyond the relatively large C₄ grazing ungulates. These would include reptiles, birds, and rodents as well as insects. Early hominids would not have competed with other large carnivores for these small animals.

This brings us to a third hypothesis for early hominid diets. Peters and Vogel (2005:232-233) support an interpretation of omnivory for the early hominids, giving the following scenario:

As a starting point we can offer the following theoretical formulation of possibilities for a 30% C₄ contribution to a subadult hominid diet based on minor potential C₄ food categories:

• 5% C₄ input from sedge stem/rootstock, green grass seed, and forb leaves
• 5% C₄ input from invertebrates
• 5% C₄ input from bird eggs and nestlings
• 5% C₄ input from reptiles and micromammals
• 5% C₄ input from small ungulates
• 5% C₄ input from medium and large ungulates

This type of formulation maximizes the diversity of food species, i.e., both food-species-richness and evenness of contribution. The exact numbers are not as important as the species richness of the formulation.

A couple of things can be noted from this scenario. First, the predominant part of the C₄ contribution comes from animal resources rather than plants. This conforms with Peters and Vogel's (2005) examination of C₄ plant resources, only few of which are both edible by hominids and potentially available in quantity in their apparent paleoenvironments. However, this dietary component does not explain the masticatory adaptations of the australopithecines (indeed, it is not intended to explain them, since early Homo does not differ in dietary C₄ contribution from earlier hominids). There is certainly nothing about the dentitions and jaw musculature of robust australopithecines to preclude an omnivorous diet of this type, but that invites the question of what fallback foods may explain that adaptation, or may explain the difference between robust and other australopithecines in that respect.

Conclusion

None of these three hypotheses really accounts for the full pattern of evidence about early hominid diets. The consensus so far appears to be that the chemical characteristics of the bones and teeth of early hominids reflect a majority diet that did not require a specialized dental adaptation. Therefore, the dental specializations of early hominids, in particular the enlargement of the postcanine dentition, reduction of the incisors and canines, and the low crowns of the molar teeth probably were adaptations to a minority of dietary intake that nevertheless was extremely important in selective terms. This would be characteristic of fallback foods eaten at times of resource scarcity, and would evidently have consisted of hard, brittle food items that could be effectively pulverized and ground by low-crowned teeth with large surface areas and thick enamel. This interpretation is supported by Ungar (2004) in an analysis of dental topography in early hominids and living hominoids (discussed in another article).

There are some remaining mysteries:

1. If australopithecines had basically similar C₄ dietary proportions, then what accounts for their differences in Sr/Ca ratios?
2. Did any A. africanus-like hominids ever coexist with a robust australopithecine species?
3. If early Homo had a C₄ proportion that came in large part from hunting or scavenging grazing species, a hypothesis also supported by their dental anatomy (Ungar 2004), then did they abandon any of the C₃ resources used by australopithecines?
4. If australopithecines were opportunistic omnivores, were there important regional differences in their dietary composition?

These questions and others might be addressed with further sampling of dental chemistry.

References:

Backwell LR, d'Errico F. 2001. Evidence of termite foraging by Swartkrans early hominids. Proc Natl Acad Sci U S A 98:1358-1363.

Grine FE. 1986. Dental evidence for dietary differences in Australopithecus and Paranthropus: a quantitative analysis of permanent molar microwear. J Hum Evol 15:783-822.

Grine FE, Kay RF. 1988. Early hominid diets from quantitative image analysis of dental microwear. Nature 333:765-768.

Peters CR, Vogel JC. 2005. Africa's wild C₄ plant foods and possible early hominid diets. J Hum Evol 48:219-236.

Schoeninger MJ, Bunn HT, Murray S, Pickering T, Moore J. 2001. Meat-eating by the fourth African ape. In: Stanford CB, Bunn HT, editors, Meat-eating and human evolution. Oxford, UK: Oxford University Press. p 179-195.

Schoeninger MJ, Moore J, Sept JM. 1999. Subsistence strategies of two savanna chimpanzee populations: The stable isotope evidence. Am J Primatol 49:297-314.

Sillen A. 1992. Strontium-calcium ratios (Sr/Ca) of Australopithecus robustus and associated fauna from Swartkrans. J Hum Evol 23:495-516.

Sponheimer M, de Ruiter D, Lee-Thorp J, Späth A. 2005b. Sr/Ca and early hominin diets revisited: New data from modern and fossil tooth enamel. J Hum Evol 48:147-156.

Sponheimer M, Lee-Thorp J, de Ruiter D, Codron D, Codron J, Baugh AT, Thackeray F. 2005a. Hominins, sedges, and termites: New carbon isotope data from the Sterkfontein valley and Kruger National Park. J Hum Evol 48:301-312.

Sponheimer M, Lee-Thorp JA. 1999. Isotopic evidence for the diet of an early hominid, Australopithecus africanus. Science 283:368-370.

Ungar P. 2004. Dental topography and diets of Australopithecus afarensis and early Homo. J Hum Evol 46:605-622.

van der Merwe NJ, Thackeray JF, Lee-Thorp JA, Luyt J. 2003. The carbon isotope ecology and diet of Australopithecus africanus at Sterkfontein, South Africa. J Hum Evol 44:581-597.

Elton and colleagues (2001) examined the record of brain size in early Homo with the following question in mind: we know that brain size increased in this lineage, but was that increase unusual compared to other lineages of primates at the same time? To answer this, they examined the brain sizes in fossil A. boisei and Theropithecus (the genus that includes living gelada baboons). Answering this question would determine whether the brain size of early Homo increased for reasons unique to this genus, or whether instead it was part of a broader trend that might be attributed to climatic changes or other ecological factors.

The results of the study showed that fossil Theropithecus showed no particular trends in brain size over time. But A. boisei did show a significantly positive trend toward brain growth over time. This trend exists whether the early KNM-WT 17000 specimen is included in the sample or not, which is important because this skull is both small and early, and by itself might create a trend in a sample that was otherwise static over time. Without that skull, the trend is still there, driven mainly by the late large skull from Konso KGA 10-525, and the early small juvenile skull Omo L338y-6. Although this latter skull is juvenile, they use an estimated adult size that is about 4 percent larger than the actual endocast.

The study compared these two cases with the evidence for brain size in early Homo. Looking only at Homo habilis, there is no apparent trend toward increasing brain size. This is partly because the largest specimen, KNM-ER 1470, is early and partly because of the great variation within the sample. The overall sample including H. habilis and early humans does show a significant trend over time, but this trend appears mainly to result from the presence of two distinct (and mostly discontiguous) species, one of which survives much later in time and therefore greatly influences the appearance of a trend. Considering early humans alone, there is really no trend evident before 1.5 million years ago, and only a slight increase up to the sample around a million years ago (Lee and Wolpoff 2002).

Some issues:

The study focused on change within each fossil species. But there is no comparison to the magnitude of changes that occurred between hominid taxa. This is problematic because most of the brain evolution in early Homo likely characterized the initial origin of the lineage from an ancestral australopithecine. It is no great surprise that H. habilis does not change markedly over time, but what is surprising is the substantial jump in size from earlier australopithecines like A. afarensis or A. africanus and later Homo. The same could be observed of the change between habilines and early humans. The authors actually run a test to see if the entire early Homo sample shows a trend over time (and it does), but it is clear from the data that the major difference is the shift in size from habilines to early humans, with each of these groups showing relatively little change over time.

The trend in A. boisei depends entirely on the earliest and latest fossils. The small size of the early Omo L338y-6 specimen is unsurprising compared to the even smaller KNM-WT 17000, so the idea that the A. boisei lineage should have changed over time is possibly expected. But Omo L338y-6 is not the smallest member of the later sample (KNM-ER 407 is smaller), so it does make a difference whether KNM-WT 17000 is excluded or not. Especially considering this is a robust probable male skull, its very small endocranial volume makes a large contrast with later A. boisei, a difference extended by many other anatomical details.

What about the late end of the sample? Here, the endocranial volume of KGA 10-525 appears very large, and is at the high end of the A. boisei range. But compared to earlier hominids, the volume is not surprisingly large. For example, the endocranial volume of AL 444-2 (A. afarensis) is estimated at around 550 mL (Holloway and Yuan 2004), and the volume of STW 505 (A. africanus) is certainly larger, perhaps over 600 mL (Hawks and Wolpoff 1999; Conroy et al. 1999). Although the body size of KGA 10-525 is not known, its molars are near the top end of the A. boisei sample, exceeded only by OH 5. This might suggest that the body size of the specimen was among the largest in the sample, and at the least we can guess that the individual was larger than the average for males.

So to address whether KGA 10-525 was surprisingly large, we have to look beyond its date and ask what the expected range of brain sizes within A. boisei would have been. Including KNM-WT 17000 at the small end, and KGA 10-525 at the large end, the standard deviation of the entire A. boisei sensu lato sample in endocranial volume is 39.3 mL. With an average volume of 480 mL, this yields a CV (coefficient of variation) of 8.2 percent.

By contrast, the H. habilis sensu lato sample, including KNM-ER 1470, has a standard deviation of 79.6 mL on an average of 634 mL, yielding a CV of 12.6 percent. So the A. boisei sample is a third less variable than the H. habilis sample.

Holloway (1980) gives CV values for recent humans, from the Danish data of Pakkenberg and Voight (1964), broken down by sex. The within-sex CV's for males and females were 8.2 percent and 8.3 percent, respectively. So the variation within the extant sample of A. boisei, including KNM-WT 17000, is about the same as within one sex in living humans. This is despite the fact that the A. boisei sample spans a million years of time and appears to have been substantially greater in body size dimorphism (as indicated by cranial robusticity and tooth sizes) compared to humans.

Tobias (1971) pools data from several earlier studies of endocranial volumes in hominoids, pooling sexes together. In his summary, the smallest degree of variation is within white-handed gibbons (Hylobates lar), where the CV of endocranial volume is 7.6 percent. Other hominoids are higher: chimpanzees at 9.7 percent, siamangs at 10.7 percent, orangutans at 10.9 percent, and a male-biased sample of gorillas at 13.1 percent. Except for the small and monomorphic gibbons, all these are higher than the estimate for A. boisei.

So the problem is not that KGA 10-525 is surprisingly large. Instead, the problem is that variation in A. boisei has likely been substantially undersampled. There should be many larger and smaller crania than have yet been found in the sample.

This is a problem for testing whether there is a significant trend within the A. boisei sample. In a sample with relatively low variation, the observation of a single large specimen at the recent end of the sample may be statistically surprising--the rarity of the large size is combined with the rarity of the recent date.

In a study of fossils, we cannot really know what the underlying variability of the extinct species was. For this reason, we are left with tests that use only the observed sample variability. The best of these are randomization tests, which randomize one or more elements of the sample to determine the likelihood that the sample would have the observed characteristics based on the data at hand. But randomization tests assume that the data themselves are sufficient to represent the variation in the underlying population. If there is good reason to think that the data are not representative, then the randomization tests may mislead about the chance that the data would be ordered in the observed way at random.

What if instead of randomly ordering the data to test its significance, instead we modeled the characteristics of the underlying population. For example, we could assume that the population had been a single species with a standard deviation similar to that observed in some living or fossil species--perhaps the observed standard deviation for earlier hominids, or for recent humans. The null hypothesis would be that this population was static in mean endocranial volume. With the computer's help, we can draw random variates from a normal distribution with the assumed standard deviation, assigning them randomly to the times observed for the real fossil sample. Then, we can perform whatever statistic we prefer upon the simulated sample, repeating the process some arbitrarily large number of times. The number of times that meet or exceed the trend observed in the fossil sample provide a p value for the null hypothesis.

What would the result of such a test be for the A. boisei sample? Good question. I'll tell you when I find out.

Why is this important?

The question is really whether the brain size increase in Homo was unique among the early hominids, or whether it may have been replicated in other species. In particular, if the brain size increase also happened in A. boisei in parallel with early Homo, that would be surprising. After all, A. boisei likely had a very different paleoecology than any member of Homo, one that was almost certainly less dependent on technology, less reliant on high-energy foods such as meat, and presenting less of a necessity for group coordination of activities. If brain size increase could occur in a significant way in A. boisei, it really raises questions about the pattern of selection on brain size in hominids.

What could explain an increase in A. boisei? One hypothesis would be energetics. The brain is a great energetic drain, because nervous tissue is very costly. For this reason, there is normally fairly strong selection in favor of smaller brains--because they are more energetically efficient. This selection for smaller brains is opposed by selection for brain functions of one kind or another, because a brain that is too small risks losing some function important for survival or reproduction.

A. boisei clearly differed from earlier hominids in its dietary adaptation, and diet determines the overall energy budget available for an organism. Suppose that the robust masticatory adaptation of A. boisei allowed the species to have a more dependable source of foods during periods of scarcity--because the range of fallback foods was extended into foods unavailable to other hominids, for example. If this were the case, then A. boisei may have had significantly less resource stress during periods of resource scarcity for other hominids, and may therefore have had less trouble meeting their energetic demands. This would mean that the selection against larger brains on the basis of their energetic disadvantages might well be weaker in a robust australopithecine. With other sources of selection on brain function the same--or even possibly increased due to a small reliance on rudimentary toolmaking or other mental adaptations--the brain would increase in size.

Some have used the apparent increase in brain size in A. boisei as an argument to address the importance of brain size expansion in later Homo. This is a point worth addressing, because it is a potentially misleading comparison. One way that it misleads is in the magnitude of change necessary to explain the apparent trends. In A. boisei, a straight regression through the earliest and latest observations indicates an increase in brain size of roughly 70 mL per million years. Of course, this regression like all others is most influenced by the smallest and largest values on the independent axis. Considering the probability that KGA 10-525 was actually larger than its instantaneous average, and that Omo L338y-6 was actually small, the actual amount of change in the species over time was likely much less than 70 mL per million years. A consideration of the data points excluding these extreme values yields a nonsignificant increase of only 21.5 mL per million years.

In contrast, the magnitude of the increase in endocranial volume in Middle Pleistocene humans is much larger. Over the past million years, humans have increased from an average of around 900 mL to the present average of around 1350 mL, for a rate of 450 mL per million years. This is at least fivefold and more probably twentifold higher than the rate in A. boisei, and does not consider the observation that the change was concentrated in the more recent Middle and Late Pleistocene. Moreover, this rate is indeed a difference between early and late average values rather than a regression including early and late extreme values. One might object that we should consider the rate of change relative to the current absolute size rather than the absolute change. From the perspective of selection and the function of brain tissue, this question is not easy to answer: it could go either way. But a strict consideration of relative brain increase as opposed to absolute brain increase still shows that recent humans increased at a rate probably seven to tenfold higher than in A. boisei. And the increase within the past 250,000 years--from approximately 1100 to 1350 mL--would indicate a much higher rate of change, at 1000 mL per million years.

So the observation of a slight trend toward higher brain size in A. boisei would not diminish the impressive degree of change in recent human evolution. Nor does it really lend to the idea that brain increases were widespread among fossil hominids and therefore unsurprising. In all likelihood there were other surprising changes, such as the increase from Australopithecus to Homo, and the increase from H. habilis to early humans. Each of these changes deserves a unique explanation, since the brain is not a character likely to increase in size at random or under the influence of genetic drift. And since the most recent increase in Pleistocene hominids occurred in every inhabited region of the world, it would require either gene flow between regions or several unique cases of simulaneous parallel evolution to explain.

Bottom line: is there anything to explain here in A. boisei? I don't really think so. The apparent trend is too likely to be generated by the outlying observations. Even if a trend existed in the species over time, it appears to have been pretty low in magnitude. This remains a case where the recovery of a single specimen with the right measurements and date would completely eliminate any statistically significant result.

References:

Conroy GC, Weber GW, Seidler H, Tobias PV. 1999. Endocranial capacity of early hominids. Science 283:9.

Elton S, Bishop LC, Wood B. 2001. Comparative context of Plio-Pleistocene hominin brain evolution. J Hum Evol 41:1--27.

Hawks J, Wolpoff MH. 1999. Endocranial capacity of early hominids. Science 283:9b.

Holloway RL. 1980. Within-species brain-body weight variability: A reexamination of the Danish data and other primate species. Am J Phys Anthropol 53:109--121.

Holloway RL, Yuan MS. 2004. Endocranial morphology of A. L. 444-2. In: Kimbel WH, Rak Y, Johanson DC, editors, The skull of Australopithecus afarensis. Oxford, UK: Oxford University Press. p 123--135.

Lee SH, Wolpoff MH. 2003. The pattern of evolution in Pleistocene human brain size. Paleobiology 29:186--196.

Pakkenberg H, Voigt J. 1964. Brain weight of the Danes: forensic material. Acta Anatomica 56:297--307.

Tobias PV. 1971. The brain in hominid evolution. Columbia: New York.