Sahelanthropus

OK, I'm going to live-blog this show. I've been looking forward to it for a while -- I loved the old NOVA series with Don Johanson and have often showed it in classes but I had to stop several years ago because it's getting out of date. These are great overview-type programs, unlike the more special-purpose one-topic shows.

The producers gave me the opportunity to review the program's script a few months ago (that's explains the acknowledgement at the end), so I'm not expecting any unpleasant surprises.

The pre-credits opening: Naked people smiling. Naked chimps grooming...

7:01: "What set us on the path to humanity? The questions are huge, but at last, there are answers..."

"For millions of years, many human-like species coexisted on our planet, until one day, there was only us."

7:03: "Apes that had walked on four legs stood up and walked on two." We see apish CGI hominins. Then, to the Sahara to see Toumaï. Michel Brunet is describing the skull.

"We, Homo sapiens, are the first ever to be alone."

7:06: To the Afar, explaining the Rift Valley and its erosive contexts. The Insta-Zoom effect across the desert is actually kind of cool. We see Zeresenay Alemseged driving an SUV, then walking in badlands with scattered bones. Nice photographs of the Dikika skull in context.

7:09: Zooming backward into a timeline, as if the years are sucking us back, the program explains the timespan of human evolution as a series of doublings backward in time.

7:10: Alemseged is in the National Museum of Ethiopia, preparing the skull. It's a nice video treatment, shoing the slow preparing with dental drill. The long shots of the postcranial elements are very illustrative -- this is a good demonstration of how the anatomy informs us about the developmental schedule and lifeways.

7:13: Don Johanson is explaining how he found AL 129-1. Then, he explains the difference between the chimpanzee and human pelvis. Too bad they couldn't have included Ardipithecus; it would be interesting.... I'm really liking the fact that you have people interacting with actual casts instead of lots of CGI images. You have a much better impression of the scale

7:15: Now the scene moves to Kenya, this is going to be about paleoenvironments. Yannic Garcin and Daniel Melnick are describing how the now-desert landscape was once much wetter. We go back to the Afar, with Alemseged explaining the fauna that's just eroding up out of the ground (wonder how set up that scene was...).

7:18: Bipedalism. It's like Saturday Night Fevur. Brian Richmond appears to explain theories about why bipedality was adaptive. This is all accompanied by contemporary dancers wiggling around. Chimpanzee-like ancestors are illustrated with video of actual chimpanzees (wonder what Lovejoy is thinking...). Dan Lieberman is talking about energy budgets. People and chimps on treadmills hooked up to oxygen meters.

7:22: Mark Stoneking explains the molecular clock. "The dates that one almost always gets are 5 to 7 million years ago for when humans and chimpanzees shared a common ancestor."

7:24: We go to Chad. Brunet explaining why they needed to recover fossils from somewhere other than East Africa. "Everyone said 'no', there just aren't any [human-like] fossils there."

7:26: "There were no bones apart from the skull..." Er...

7:27: The skull is reconstructed with a CT scanner and then cast. Oops...the rest of the shots of casts are all taken directly from the skull, not the 3-d scan version. Nice artist's rendering of Toumaï here.

7:30: I'd hate to be one of the dancers walking by on the screen with the voiceover, "Walking upright didn't mean that they had big brains."

7:33: Brain growth in Selam. Hints of a longer childhood -- of course, at 330 cc, it's almost the size of a full-grown chimpanzee. Todd Preuss is discussing the evolution of the brain, showing us actual pickled brains of human and chimpanzees. Lunate sulcus -- was Selam like a human or a chimpanzee?

7:35: Ralph Holloway is describing the brain reorganization -- great shot of him with his collection of endocasts. The conclusion is that the lunate sulcus was human-like.

7:37: Now we have stone tools appearing, Brian Richmond explains how we recognize tools. Unlikely they were made by Australopithecus, because they didn't make them earlier. Skip forward to KNM-ER 1470, "the dawn of a new era, beginning around 2 million years ago." Tools were used for meat processing. Homo habilis was small in body size, but had a much bigger brain than Australopithecus.

7:41: Viktor Deak is reconstructing Homo habilis. I like it, more apish than the usual rendering.

7:43: "Africa's gradual drying trend was punctuated by bursts of rapid climate fluctuation." We see Rick Potts explaining the stratigraphy of a lake alternating with desert and volcanic layers over time. The idea of "variability selection" is explained.

7:45: Analyzing diatoms in layers of rock -- the species tell the alternation of shallow and deep lake levels. It's a record of strong fluctuations. We see rapid clips of three different scientists (Potts, John Kingston, and Mark Maslin) talking about water fluxes. It's a good way of explaining the climate instability -- although they could have gone a bit further: when they mention "Lake Victoria-sized lakes appearing and disappearing", for example, they might have pointed out that Lake Victoria itself has appeared recently.

7:48: Dust from ocean cores. Once again, it comes down to tiny sea creatures whose anatomy correlates with date.

7:50: We get a rapid montage reviewing the climate instability idea. Hmmm...I have to say that the very fast cutting of clips and louder music doesn't really add to the credibility of the idea -- it seems like something is being left out.

7:51: Rick Potts restates the variability selection argument. "Simple but revolutionary idea -- human evolution is nature's experiment with versatility...we are creatures of climate change."

That's the end. I think the paleoenvironment story was well done. The shots of how this science is done were very illustrative -- from the field to the lab, the program showed the fine layers of sediment and careful study of microscopic creatures.

On the other hand, the show may have gone a little too far in the "climate made everything happen" direction. I don't think the "variability selection" idea explains the origin of Homo, and while the program did briefly list alternative views about the adaptive value of bipedality, it left no doubt that African desiccation and loss of forest was the ultimate cause.

I think everything with actual fossils, dirt, or rocks was well done. In particular, we got a good view of most of the Selam skeleton, with the notable exception of the hyoid bone. These are the best available images of the specimen to date. Holloway's descriptions of endocast evolution were well done, placed in the middle of a big table of fossil casts. I like the solidity with which the program showed the fossil record. Hopefully the next two segments will also follow this technique -- much preferred over the CGI-reconstruction technique.

I will be out of the country for the next two parts of the trilogy, so I'll have to see if I can get them online. The NOVA Evolution website has the first episode online now, so there's some hope.

Some weeks ago, I wrote about an article by Alain Beauvilain and Jean-Pierre Watté, in my post, "Sahelanthropus: Did camelherders bury Toumaï facing Mecca?" If you missed that post, go back and read it -- it gives some essential background.

I ended the post with this little observation:

Toumaï's skull was found alongside a femur.

I imagine that a majority of paleoanthropologists have heard that the faunal collection from Toros-Menalla includes a primate femur of the right approximate size to match the Toumaï skull. Probably only very few knew that this femur may have been found in the immediate locality of the skull. Still, a lot of them must be wondering: If there are possible postcranial remains of Sahelanthropus, wouldn't they be the most important test of whether the species is the first hominid?

Now, thanks to a story in the July print issue of the French science magazine La Recherche, along with some valued correspondence from readers, it's possible for me to give some more details.

Now if you really want to beat the science press, it helps to have readers who take really obscure journals.

I haven't written much here about Sahelanthropus. In 2002, I joined a number of other people who doubted the evidence for bipedalism in what was then (and has since been) touted as the "earliest known hominin." Maybe it is, maybe it isn't. But we weren't convinced by the evidence. Dental similarities with early hominids were also shared with a number of Miocene ape genera, while the evidence for vertical posture, based on the position of the foramen magnum, seemed weak. We made our case in a 2004 paper in PaleoAnthropology, which is open access. Since no new evidence has come to light (or at least, to print), that's where matters stand as far as I'm concerned. I still think the evidence for bipedality in Sahelanthropus is equivocal, and that the specimen's date may be too old to be a member of the hominin lineage.

Meanwhile, also in 2004 began a strange series of events involving Alain Beauvilain, a geographer working with the original Sahelanthropus excavation project. I have no personal knowledge of the details, aside from the published record -- so that's what I'll stick to.

Yes, this story does end with camelherders burying fossils....

Hey, I never said it was a vulgar ape...

A fresh storm has broken out over an ancient fossil presented by its defenders as a forebear of humanity and dismissed by its critics as the remains of a vulgar chimp. Controversy has swirled around Toumai, the name given to the nearly-complete skull, ever since it was found in the Chadian desert in 2001.

...

But the man who discovered Toumai, Alain Beauvilain, of the University of Paris at Nanterre, has now publicly challenged [its 7-million-year-old date] estimate.

This really isn't a very well-written story (it refers to "carbon dating" the remains, for instance). I suppose that if Beauvilain is correct, the true date should likely be younger, but that doesn't really affect anyone's interpretation of the skull. The only practical effect: If we were to assume it's a hominin (which I don't), then a younger date would reduce the apparent discrepancy with the relatively recent genetic divergence between hominins and chimpanzees.

The rate of neutral mutations varies across the genome. When studying a single gene, this variation in rates is not especially important -- it is generally possible to obtain an estimate of the neutral rate for a single locus by comparing just that locus among closely related species.

But some comparisons involve looking at the pattern of variation among different loci. For instance, testing hypotheses about the ancestral populations leading to living species (like the common ancestor of humans and chimpanzees) involves comparing the amount of divergence among many independent loci. The variance in divergence times among loci gives an estimate of inbreeding in the ancestral population.

I discussed this particular example two years ago this week, after the paper that proposed extended hybridization between ancestral hominids and chimpanzees. The conclusion of the paper was that the X chromosome displays much less divergence between humans and chimpanzees than the autosomes, and this might reflect a late introgression of the X chromosome into hominids from another population that (mostly) was ancestral to chimpanzees. The autosomes, by contrast, averaged very old genetic divergences, although there was substantial variance. As I concluded then, the data look consistent with a large population size in the human-chimpanzee ancestor species, coupled with greater selection on the X chromosome. The interpretation of large population size (or alternatively, the interpretation of long-term population structure) comes from the low inferred inbreeding in that ancestral population -- which caused the variance in divergence dates among loci.

But there is another reason for a large variance in divergence dates: variance in mutation rates. Whenever mutation rates vary among loci, this variance adds to the variance among loci in their between-species genetic differences -- that is, the substitution rate. And as long as we are excluding selected sites (as we always try to do for these kinds of comparisons) we will overestimate the genetic diversity in ancestral species whenever the mutation rate varies among loci.

A new paper by Svitlana Tyakucheva and colleagues looks at human and macaque genomes to find patterns underlying the variance in mutation rates among regions of the genome. They find that a number of factors may cause such variations, including chemical factors like the CG content of the genome, functional causes such as male versus female rates of recombination, and large-scale structural causes such as telomeric proximity:

While a complete understanding of all biological mechanisms leading to variation in neutral substitution rates across the genome remains elusive, it is plausible that at least some of these mechanisms are conserved over relatively long evolutionary distances. For instance, both mouse-specific and rat-specific substitution rates are positively correlated with rodent-primate substitution rates [14], suggesting shared mechanisms persisting over ca. 90 million years [15]. Additionally, a positive correlation exists in substitution rates of homologous X- and Y-chromosomal introns that diverged from each other ca. 100 million years ago [16] (Tykucheva et al. 2008: R76).

Their finding that male recombination is an important contributor to mutation rate heterogeneity puts the focus on the X chromosome -- which has little recombination in males -- as unusual. X versus autosomal position did not explain a large fraction of the variance in this study (only around 2 percent, controlling for other factors) but the deviation was in the right direction to help account for the low X chromosome divergence between humans and chimpanzees.

Altogether in this study, a large fraction of variation in the human-macaque substitution variability could be explained by phenomena that affect the rate of mutations, including the structural and functional factors listed above as well as the corresponding homologous variability between mice and rats, and dogs and cattle. If these variations were explained by inbreeding in the human-macaque ancestral species, they would be random with respect to the dog-cow or mouse-rat divergences, and with respect to structural causes. So current estimates of the effective sizes of human-chimpanzee and other ancestral populations are almost certainly inflated. The amount of inflation is not clear, but a good estimate will require correcting for a large number of factors -- a complicated analysis.

Since the date of the human-chimpanzee divergence depends on our assessment of the diversity within the human-chimpanzee ancestral population, it may be a while before we can settle the issue of human-chimpanzee divergence time. That may or may not provide hope for Sahelanthropus, Orrorin, and Ardipithecus kadabba -- all supposed hominids that would predate 5 million years ago, the current best genetic estimate of the human-chimpanzee divergence time. To be sure, if the date is simply in error, that error might encompass older dates consistent with a 7-million-year divergence. But I'm not sure we should believe that the error is biased toward an older divergence -- "error" might lean in either direction, and a younger species divergence remains possible.

References:

Tyakucheva S, Makova KD, Karro JE, Hardison RC, Miller W, Chiaromonte F. 2008. Human-macaque comparisons illuminate variation in neutral substitution rates. Genome Biol 9:R76. doi:10.1186/gb-2008-9-4-r76

There's nothing especially surprising about the functional interpretations in Richmond and Jungers' paper about the Orrorin BAR 1002'00 femur. They conclude it was an australopithecine-like biped, because it shared several features with australopithecine femora: in particular, it has a long, narrow, anteroposteriorly flattened neck and a broad thick proximal shaft.

In this, they mirror the conclusions of the original description of the Lukeino fossils by Senut et al. (2001). Richmond and Jungers also reiterate the evidence for arboreality in the Lukeino fossils, including the well-developed musculature of the distal humerus and the chimpanzee-like curved finger bone. I wonder why their analysis could not have made something more out of the other two femoral fragments, one of which is fairly large (but lacking the head). Still, the paper reiterates the quite good evidence for bipedality in the most complete femoral specimen.

I wonder sometimes how closely people actually read the papers they comment on. The associated coverage, including Ann Gibbons' article, has made a lot out of a small point in the paper, but I think that the commenters have it wrong.

Here's the story: When the Orrorin materials were first published, Brigitte Senut and Martin Pickford put forward the argument that these may be more closely related to Homo than to known australopithecines. They based their argument mainly on Orrorin's relatively thick-enameled molars, which they viewed as different from the thin-enameled molars of Ardipithecus, but lacking the enlarged dentition of Australopithecus. So, they suggested that Orrorin might be a plesiomorphic ancestor of Homo, and that Ardipithecus and Australopithecus represent divergent lineages derived in their dental anatomy.

I don't find that suggestion very compelling, because it seems to put too much faith in the absence of evolutionary reversals. There's no reason why a large-molared australopithecine should not have given rise to small-molared Homo, particularly since smaller-toothed Homo habilis is apparently derived from earlier, larger-toothed "Homo" specimens like A. L. 666-1 and Omo 75-14. And Haile-Selassie, Suwa and White (2004) claimed that the Orrorin, Sahelanthropus, and Ardipithecus dentitions were so similar that they might represent one taxon. So the dental contrasts among these early hominids are probably not great enough to justify the idea that Orrorin is an exclusive Homo ancestor.

The femur also formed a part of this phylogenetic story, with Senut and Pickford having noted the lack of extreme australopithecine-like features in the femur. The Orrorin femur has a less exaggerated neck length than many australopithecine specimens, it is larger than many, and appears to have a higher neck-shaft angle. To the extent those features differ from later Australopithecus, they resemble the human anatomy.

Richmond and Jungers address this argument very briefly in their last paragraph, by noting that the functional elements of the Orrorin femoral anatomy are entirely consistent with the australopithecine pattern of bipedality:

The similarity between O. tugenensis and australopith femora weakens support for scenarios in which O. tugenesis is ancestral to Homo to the exclusion of A. afarensis (4). Instead, the overall primitive hominin morphology of the O. tugenensis femur, along with primitive dental anatomy, is consistent with the more parsimonious hypothesis that it is a basal member of the hominin clade.

I think that's fair, as far as it goes. The overall morphological pattern of this femur, with its long neck and broad shaft, is much like known australopithecine femora. But to go a bit further, their metric comparisons show BAR 1002'00 to be the most Homo-like of the early hominid femora they examined, and their phenetic cluster puts it basal to the other australopithecines. That's pretty much exactly what Senut et al. have consistently said. So I have a hard time understanding how those observations refute the idea that Orrorin has a more Homo-like femur than later australopithecines!

Again, I don't put much stock in the phylogenetic argument for an Orrorin-Homo link. I don't see any difficulty deriving Homo from Australopithecus, especially given the likely effects of body size evolution on the locomotor pattern. And at least one or two early Homo femoral specimens, like KNM-ER 1481, share most of the Australopithecus-like pattern of proximal femur anatomy. But this paper surely doesn't add anything new to the critique of Senut and Pickford's preferred phylogenetic hypothesis. The details simply don't detract from their story.

References:

Richmond BG, Jungers WL. 2008. Orrorin tugenensis femoral morphology and the evolution of hominin bipedalism. Science 319:1662-1665. doi:10.1126/science.1154197

Gibbons A. 2008. Millennium ancestor gets its walking papers. Science 319:1599-1601. doi:10.1126/science.319.5870.1599

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

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

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!

That depends on whether these teeth are really from a gorilla, I suppose.

Oh yeah, sure, "saved paleoanthropology" is overdramatic. But what am I supposed to write? Over four years, we have had a series of genomic comparisons narrowing down the age of the human-chimp common ancestor to something like 2/3 the age of Sahelanthropus. I said it was a crisis, and it is: these data sources must agree. Either we have to cast out a bunch of hominids, or we have to wrench the genes by around a factor of two.

Out of this week's Science Times special on evolution, I clicked into John Noble Wilford's article first, titled "The Human Family Tree Has Become a Bush With Many Branches".

Now, I don't know about you, but that seems like a boring headline to me. They've been talking about human evolution being a bush for going on 20 years now. It was an old idea when I was in graduate school. So it seems like, if this is all we have going on, the "new frontier" of paleoanthropology must be pretty dull.

The writer doesn't write the headlines, and the headline doesn't describe Wilford's story, which is basically a verbal slide show of fossil discoveries over the last decade or so. Some bone pictures (of the actual species discussed) accompany the article, and it's a good enough sort of account of new finds since 1990, framed around the tension between fossil finders and molecule mavens.

But I'll be a little critical. The thesis is that paleoanthropologists suffered a crisis of confidence after molecular data came online in the 1980's, and "a rapid succession of fossil discoveries since the early 1990's has restored" it.

Well, OK, maybe. But consider the listed discoveries: Kenyanthropus, Ardipithecus ramidus, Ardipithecus ramidus, Orrorin tugenensis, Sahelanthropus tchadensis, Homo floresiensis, and Australopithecus anamensis. Of all of these, only Ar. ramidus and Au. anamensis have gone without significant controversy.

We can set aside H. floresiensis for a moment -- the controversy about it being possibly the loudest, it also stands apart as the only species listed younger than 3.9 million years. All of these early Pliocene and Miocene species have also been challenged -- by the discoverers of the others, by old hands, and by young upstarts like me. At least one research group has claimed that all of the Miocene "genera" may actually belong to one species. Another has claimed that most of these "hominids" may actually be apes.

Whether there was any crisis of confidence among paleoanthropologists, all this disagreement is certainly business as usual.

And, contrary to the article, every one of these species would be thrown from the hominid line, if we believe the molecules. Here's the text from the article:

Genetic clues also set the approximate time of the divergence of the human lineage from a common ancestor with apes: between six million and eight million years ago.

Fossil researchers were skeptical at first, a reaction colored perhaps by their dismay at finding scientific poachers on their turf. These paleoanthropologists contended that the biologists' "molecular clocks" were unreliable, and in some cases they were, though apparently not to a significant degree.

...

The new finds have filled in some of the yawning gaps in the fossil record. They have doubled the record's time span from 3.5 million back almost to 7 million years ago and more than doubled the number of earliest known hominid species. The teeth and bone fragments suggest the form -- the morphology -- of these ancestors that lived presumably just this side of the human-ape split.

It is true that the new fossils date as far back as 7 million years; with Sahelanthropus just under that date, Orrorin at around 6 million, Ar. kadabba at 5.5, Ar. ramidus at 4.4, and Au. anamensis at around 4.1.

But it has been many years since a genetic comparison indicated a human-chimpanzee common ancestor as old as 6-8 million years. This year's study by Holbolth et al. (2007) estimated a human-chimpanzee speciation time of 4.1 +/- 0.4 million years. That makes Au. anamensis possibly too young to be a hominid. The rest of those species would presumably be just so many apes.

Now, I don't believe for a second that Au. anamensis is an ape and not a hominid. It just looks too much like Au. afarensis -- so much so that some would put them in the same species. The evolutionary transition between these two is well documented, and will be more so when some as-yet-unpublished fossils come out. So anything younger than 4.1 million years is almost certainly not right for the human-chimpanzee divergence.

But the 4.1 million year estimate is not unusual compared to other recent studies. My post from last May covers many of these recent studies, including last year's problematic "hominid-chimpanzee hybrid speciation" paper by Nick Patterson and colleagues. The conclusion in that paper about hybridization was certainly wrong, but the date of 5 million years was right in line with other estimates.

These genetic comparisons are not easily dismissed. Possibly there has been a rate deceleration of mutations in the human lineage that means that the estimated dates are too recent. Maybe 4.1 million years can be stretched into 6 million. Maybe it can even be stretched into 7 million. But all this stretching does have other effects -- on the estimated dates of earlier divergences -- and those are compounded by a large multiple of the few million years we may try to push the human-chimpanzee speciation date. That 4.1 million year estimate is calibrated from an African-Asian great ape divergence at 18 million years ago. Push the human-chimpanzee divergence to 7 million, and you push the orangutan-human divergence back into the Oligocene. Are silent sites in humans evolving more slowly than cercopithecines? Probably. Are they evolving that much slower than orangutans? I suppose nothing is impossible, but maybe we should take another look at those fossils.

All this is to point out that there really is a conflict between these Miocene "hominids" and genomic evidence about human-chimpanzee speciation time. I don't see any magic solution to this problem from the molecular side -- those dates keep coming up again and again from different regions, and from comparisons across many regions -- including estimates that are not calibrated by other fossil divergences. This is not an easy "the molecular clock must be wrong" kind of problem.

Nor are the fossils an easy problem. There is pretty good evidence for vertical posture or hindlimb-dominant movement in all of these "hominids." Up to now, we've accepted these kinds of features as de facto evidence of bipedality, and assumed that bipedality is such a unique character of hominids that it is unlikely to be any older. Yet few of these fossils provide really good evidence for obligate bipedality, and some of them provide none at all.

Is it possible that bipedal apes long preceded the divergence of humans and chimpanzees? Was the common ancestor of the two lineages a biped? Or was significant vertical posture a common feature of many Miocene apes -- making Sahelanthropus a possible homologue of Oreopithecus?

Which feature is the important one? The long nuchal plane of Sahelanthropus? The femur neck cortical bone distribution of Orrorin? The toe bone of Ar. kadabba? Heck, I can hardly convince my undergraduates about that toe bone!

I've talked to people about this. Some think that all the molecular stuff is just jibberjabbing, and any day now we will find out that the date estimates were wrong all along.

I think it may be time to start doubting our confidence again.

UPDATE (6/28/2007): I've gotten into rather an interesting e-mail discussion about whether I should have included Homo georgicus on the list of new species. Frankly it didn't occur to me: Wilford didn't mention it.

Actually if you start to think about all the new names that have been proposed in the last 15 years, it is a quite bushy list. It will be no surprise that I think this bushiness has more to do with the listers than the listees.

Anyway, there is something interesting about early Homo right now that goes beyond the simple splitter/lumper questions. I'll have more to say about it in a few days.

References:

Hobolth A, Christensen OF, Mailund T, Schierup MH. 2007. Genomic relationships and speciation times of human, chimpanzee, and gorilla inferred from a coalescent hidden Markov model. PLoS Genet 3:e7. doi:10.1371/journal.pgen.0030007

Patterson N, Richter DJ, Gnerre S, Lander ES, Reich D. 2006. Genetic evidence for complex speciation of humans and chimpanzees. Nature 441:1103-1108doi:10.1038/nature04789

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

Well, I guess they've got a plot for the pilot of that caveman show:

Humans caught pubic lice, aka "the crabs," from gorillas roughly three million years ago, scientists now report.

Rather than close encounters of the intimate kind, researchers explained humans most likely got the lice, which most commonly live in pubic hair, from sleeping in gorilla nests or eating the apes.

"Sleeping in gorilla nests." Yep, that's the ticket.

The quote is from a LiveScience article by Charles Q. Choi. The article talks a lot about "monkey business" but really spends more time on the hominid-eating-gorilla scenario:

"Unfortunately, even today among modern humans there's a bush meat trade where gorillas are killed for their meat," he said. "If archaic humans were butchering or scavenging those animals 3.3 million years ago, it would be a simple thing to transfer those lice from prey to predator."

UPDATE (3/7/2006): Carl Zimmer's post is great (he's all about the parasites) and mirrors some of what I wrote below. He also includes probably the best snarky quote: "Is this evidence of a Pliocene love that dare not speak its name?"

To telegraph my conclusion a bit, I still think the flawed assumption is that the hominid-gorilla interaction occurred when the hominid and gorilla Pthirus diverged. The interaction works a lot better later, assuming within-gorilla parasite variation. Since there is a lot of within-human variation in the other louse genus, Pediculus, the idea of a couple million years of delay between louse genetic divergence and lateral transfer is not at all unlikely, even without invoking ancient gorilla speciations.

Thoughts

I downloaded the research paper in BMC Biology by Reed and colleagues. Here's the 'Conclusions' section of the abstract:

Reconciliation analysis determines that there are two alternative explanations that account for the current distribution of anthropoid primate lice. The more parsimonious of the two solutions suggests that a Pthirus species switched from gorillas to humans. This analysis assumes that the divergence between Pediculus and Pthirus was contemporaneous with the split (i.e., a node of cospeciation) between gorillas and the lineage leading to chimpanzees and humans. Divergence date estimates, however, show that the nodes in the host and parasite trees are not contemporaneous. Rather, the shared coevolutionary history of the anthropoid primates and their lice contains a mixture of evolutionary events including cospeciation, parasite duplication, parasite extinction, and host switching. Based on these data, the coevolutionary history of primates and their lice has been anything but parsimonious.

There is actually a much more interesting story here than is indicated in either press account or abstract. The genera Pediculus and Pthirus were thought to have diverged at the time that gorillas diverged from the chimpanzee-human clade. This would explain why gorillas have Pthirus and chimpanzees Pediculus. The fact that humans have both ... well, that remained unexplained. The purpose of the study was to test whether humans retained the two genera ancestrally, or if instead they picked one up later.

What they found is that the two genera didn't diverge at the gorilla-chuman split, but instead way earlier. Their estimate for the Pediculus-Pthirus divergence is 13 million years. Thirteen million is as much as twice the age of the human-gorilla common ancestor. This estimate is probably biased toward the recent side, since it is calibrated against a divergence between hominoid and baboon lice assumed at 22.5 million years ago -- probably more recent than the true hominoid-baboon divergence.

The paper considers it likely that the human-gorilla-chimpanzee common ancestor lineage maintained this pair of lice species for the intervening time period, with one genus being lost in each of the two (gorilla and chuman) descendant clades. This ancestral lineage would be similar to humans in that respect -- host to two distinct parasite lineages, both of which stemmed from a single ancestor species.

But much later than the chimpanzee-human divergence, humans apparently picked up the gorilla lice somehow. The paper doesn't belabor this point or attempt to explain it, beyond this:

Evidence suggests that Pthirus pubis has been associated with humans for several million years, and likely arrived on humans via a host switch from gorillas. Despite the fact that human pubic lice are primarily transmitted via sexual contact, such contact is not required to explain the host switch. Parasites often switch from a given species to a predator of that species [17], and are sometimes found to switch to unrelated hosts in communally used areas, such as roosting or nesting sites [18]. The host switch in question could have resulted from any form of contact between archaic humans and gorillas including, but not limited to, feeding on or living among gorillas. Regardless of how the transfer occurred, suitable habitat had to be available on the new human host for the host switch to be successful. For example, it is possible that the switch of Pthirus from gorillas to humans coincides with a change in available niche space in humans, such as the loss of body hair. Further study, however, is required to test such a hypothesis (Reed et al. 2007:7).

Hominids were certainly not hunting gorillas 3.3 million years ago. At least, not the hominids we know about. That date is a bit older than Lucy; it's 700,000 years older than the earliest evidence of flaked stone and 800,000 earlier than the earliest evidence of antelope butchery. Hominids weren't hunting gorillas because they weren't hunting any large mammal species then.

What's worse, gorillas and hominids weren't sympatric 3.3 million years ago. At least, not the gorillas and hominids we know about. Unless gorillas ranged into open woodland, and in particular the East African coastal forest, or hominids ranged into the central or west African rain forest, they never came into contact with each other at all.

If anything, we might expect that gorillas and chimpanzees would have been likely to come into contact and exchange parasites. They are currently sympatric, they eat the same foods, and they even build similar sorts of nests. It's like they share the same locker room. But they didn't have this parasite exchange.

It's all very strange. First we have this long period of divergence of the two great ape louse genera (orangutans don't have their own louse species). Then we have a divergence of the human and chimpanzee Pediculus species just exactly when it should have happened. And then there is this lateral transfer of lice from gorillas to humans 3 million years ago - when hominids and gorillas weren't apparently sympatric and had no credible mechanism for lice exchange.

Here's my hypothesis: cryptic African hominoids. The apparent craziness all comes from the assumption that the only species that existed are the ones we know about. For Africa 3 million years ago, that means two or three hominid species, one gorilla lineage and one chimpanzee lineage. We don't have any fossils that old for the apes; we can only infer their existence from the fact that they exist now.

Let's consider what we know. We know that 3 million years ago there weren't any chimpanzee or gorilla relatives in the Rift Valley, and plausibly (but not definitely) not in South Africa or the Sahel.

We don't know how extensively hominids ranged into the west African or central African forests, particularly from the north and southeast. We don't know how extensively gorillas and/or chimpanzees may have ranged outside the core forested areas where they have historically existed. In the absence of Homo, the competition between these apes and hominids at the forest boundaries may have been a close game.

We don't know how many species of ancient chimpanzees and gorillas there may have been. The present subspecific variation of chimpanzees seems to reflect recent colonization of the eastern range from central Africa, and some substantial population interchange between central and western ranges. Gorilla subspecies now seem to have emerged within the same time frame, with a possible colonization from their western range into their eastern range within the past million years.

Bonobos are only ca. 850,000 years old (Won and Hey 2005). To summarize, the current eastern chimpanzees weren't in East Africa half a million years ago, and the bonobos weren't south of the Congo a million years ago, and eastern gorillas weren't there a million years ago either.

Who was? It seems to me that the best candidates would be ancient species of gorillas and chimpanzees that no longer exist. A second-best (and maybe more interesting) candidate is some variety of hominid. A third-best (and even more interesting) candidate is an ancient ape lineage dating from before the G-C-H divergence.

Three million years ago, any one of those possibilities is credible. Here's my favorite: two gorilla species (or subspecies) became isolated enough for louse divergence 3.3 million years ago, and continued to coexist. Sometime after 2 million years ago, Homo encountered one of these species and picked up its lice. That gorilla lineage later became extinct, perhaps by range expansion from Homo.

Oh, and the long divergence time between the two lice genera? I like a long divergence and later lateral transfer from some pre-H-C-G Miocene ape lineage. There were likely several in Africa to choose from. Maybe it was Sahelanthropus...

References:

Reed DL, Light JE, Allen JM, Kirchman JJ. 2007. Pair of lice lost or parasites regained: the evolutionary history of anthropoid primate lice. BMC Biol 5:7. doi:10.1186/1741-7007-5-7

Won Y-J, Hey J. 2005. Divergence population genetics of chimpanzees. Mol Biol Evol 22:297-307.

It's a hazardous business, making predictions -- all the moreso because New Year's predictions have a deadline. If they don't happen this year, well, that's too bad, because we'll be checking back a year from now to see how well you did.

Last year, I did pretty well. My 2006 predictions are listed below. I ordered them originally "from most certain to most speculative". As you can see, the first five (i.e., the more "certain" ones) all came true; the last five (i.e., the wild-arsed speculations) didn't. So let's check them out:

• 10. We will see a name for the Flores pathology. OK, we got several names, and the issue is far from settled, but this was the year that the Homo floresiensis doubters struck with their papers on the remains.
• 9. There will be two Neandertal genome-related announcements. I undercalled this, since there were three -- the initial announcement in June of the Neandertal Genome project, the announcement and publication in November of the initial sequence results, and the announcement about possible introgression of microcephalin.
• 8. No Ardipithecus. Sometimes, predictions write themselves.
• 7. "Population cluster" will become the new "race". This one is debatable, but enough papers on multi-ethnic SNPs have used the term this year, that I think it is emerging as the replacement for the race concept for a certain class of geneticists. I expect it will continue -- "cluster" has such a neutral computer-program-centric connotation, that people like to use it.
• 6. There will be another paper (yes, besides the one last month) using genetics to estimate the time of the human-chimpanzee divergence. The date will be 5 million to 7 million years ago. Oh, my. There have been bigger messes than the Patterson et al. 2006 paper, but not many. Yes, it was yet another paper with a 5-million to 7-million-year-old divergence, but it had so much more!
• 5. Evidence of recent selection will be found for several Y chromosome genes. Wishful thinking or prediction for the next year? You decide!
• 4. Sahelanthropus postcrania will be published. This one didn't happen this year, but I'm carrying it over onto the 2007 list.
• 3. There will be an ancient DNA announcement from China. Someday it will happen, but not this year or next.
• 2. StW 573 will be proposed as a new species ancestral to all later hominids. Well, we got the opposite -- with a new younger date, StW 573 was proposed as the ancestor of...nobody! Which was by far the smaller of the redating stories this year.
• 1. A Hawks weblog post will be cited in a peer-reviewed research paper. We can only hope this happens in the coming year, but carrying it over just seems desperate...
• BONUS: A new Georgian hominid will be a robust australopithecine. I still think somebody will find an australopithecine outside Africa in the next decade, but it's not to be from Dmanisi -- the hominids are too localized in a single feature.

So that should give some indication of how to read the list for the next year. I'm listing from more certain to more speculative again, and again I'm excluding most of my own work. The main effect of this is just that I'm not including secrets that I know will be coming out this year. Once again, the predictions are Delphic -- if only I were cleverer, I could make them come out right no matter what!

• 10. Sahelanthropus postcrania will be published.
• 9. Two words: Holocene 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.
• 7. The mitochondrial history of human dispersals will become more and more detailed, but no paper will test against other loci.
• 6. Another (yes, another) paper about the chimpanzee-human divergence will peg it between 5 and 7 million years ago.
• 5. Three papers with new Ethiopian fossils.
• 4. Another early Upper Paleolithic specimen will emerge from a museum collection.
• 3. A big year for Miocene apes, which will look increasingly important in the story of human brain evolution.
• 2. Maturation rate in early Homo becomes a dead issue, because of the variation in dental and skeletal maturation in living people.
• 1. The year will end without a single new hominid species having been named.
• BONUS: A dramatic development in the problem of pre-2.0-million-year-old Homo.

I ended the year with just a shade fewer than 1 million visits since last January 1. The Neandertal women brought me over 10,000 readers in a single day -- the most ever. I know a few of the big stories from the coming year, but there will be many more that nobody can predict. There's no doubt in my mind that 2007 will be a big year!

Despite all the trouble I had traveling (or maybe because of it), I got to have a really enjoyable time finishing Ann Gibbons' new book, The First Human. For a while I was really afraid I'd lost it in the backpack without knowing how it ends! But what a relief, it was in another suitcase so I can report on the whole thing.

I've read most -- not all -- of the recent trade books about paleoanthropology, and this is definitely one of the top few in terms of being fun to read. It follows a familiar form: the quest for the source of the Nile. The book even mentions Burton and Livingston, whose explorations were to some of the earliest anthropologists what the Leakeys discoveries were to the current generation. Like the quest for the solo transatlantic flight, the summit of Everest, or the race to the Moon, the paleoanthropologists here all are trying to capture the same prize: the earliest hominid.

The book appeals in large part because it is well-written. Instead of beginning with the long dry history of finding bones in old dry places, Gibbons' first chapter plunges us right into the middle of three discoveries of the mid-1990's -- all happened within six months of each other, but the events of January 1995 brought them together. The chapter even ends with a cliffhanger!

Then comes the long dry history, with the usual cast of characters: Haeckel, Dubois, Dart, Louis and Mary Leakey. I was apprehensive about this -- no book ever seems to skip this stuff, and it's usually the same boring slog -- but Gibbons adds some details that most people haven't seen before. She's mercifully light on the "Dart courageously fighting the scientific establishment" theme, and brings us a great description of Dart excitedly opening the crate containing the Taung fossils at a friend's wedding. We get rather less of Louis Leakey's long struggle for recognition and more of his behind-the-scenes support from LeGros Clark.

Most notably, Gibbons brings us sketches of many of the paleontologists that the usual accounts miss. We see Bryan Patterson find not one, but two of the earliest hominids, and the episode that caused him to leave Kenyan field work, with his site of Kanapoi lying fallow for 30 years. We are led down the blind alley of Ramapithecus with Elwyn Simons and David Pilbeam. And we follow Yves Coppens to the Omo, Hadar, and Chad. Indeed, one of the real highlights is the account of field research in Chad, which I haven't seen described elsewhere in English so well.

The soap opera really begins with the origins and education of the current fieldworkers, who are as interlinked as characters on Days of our Lives. Pilbeam plays a Kevin Bacon-like role connecting Michel Brunet, Andrew Hill, and Martin Pickford. Pickford and Richard Leakey were old schoolmates, and -- maybe or maybe not, according to the book -- Hill comes between them. The chief fossil hunter from Hill's team goes to work for Pickford. The son of the chief fossil hunter for Richard and Maeve Leakey goes to work for Hill.

We see quite a bit less of the soap opera in Ethiopia, which describes the current Middle Awash work extensively but has little to say about Hadar or other current field sites. Donald Johanson's perspective on events of the last twenty years is very noticeably absent. We see Mary Leakey's anger at White and Johanson for naming her Laetoli discoveries Australopithecus afarensis, but the section does not explain the justification for the anger -- attaching the name to LH 4 as the type specimen removed any chance of naming the Laetoli hominids anything else.

Ian Tattersall raised an important point in his Nature review of the book: Any reporter who depends on access to subjects faces a possible conflict of interest. Report bad things about the subjects, and they may restrict access. Gibbons has obviously received exceptional access to some of the book's subjects -- indeed, the book mentions the famous lack of journalistic access to some of the research teams. Has this exceptional access affected the narrative?

I think that the book has a fair account of many events, but omits other well-known incidents that might have been described. For most of these, there is little that Gibbons could have done -- after all, if some subjects don't talk to you, and others won't give details about certain events, then what are you going to write about? In fact, there must be an intense incentive for many people not to cooperate with a book like this, especially those hoping to continue fieldwork in Ethiopia or begin there in the future. The accounts that are in the book make quite plain that one misplaced word can result in field permits being revoked, or access to collections being revoked, or even worse. As a result, the book puts on the record many arguments that were aired in public -- like the dispute over the Galili field site, for instance -- but doesn't necessarily give the whole story.

There is pretty obviously one overarching prize that shapes the entire narrative. The introductory chapter ends with the world on Alan Walker's "tenterhooks" -- in 1995! -- waiting to see the Ardipithecus skeleton. The book describes on four occasions just how fragile the skeleton was. Twice we hear how the condition of the skeleton "tempered" the Middle Awash team's excitement, twice it is described as "the most fragile skeleton ever found," twice as "roadkill." Early in the book White emerges as a secretive Svengali; at the end -- during an event White himself describes as "theater" -- we see him casting aside the velvet curtains to show his specimen at last to his skeptical colleagues.

Except, well, we don't get to see it. A reader might be forgiven for thinking the obviously crushed skull on the book jacket is the centerpiece of the book -- its "crushed" skull is twice mentioned. Sadly, no, the cover shot is just Sahelanthropus. Ardipithecus is still locked in its fortress of solitude, unseen by the unwashed. This does raise some concern for me -- since Gibbons will undoubtedly be writing the story of this fossil when it at last surfaces.

But some of the best moments are those that shine light on the relationship of the science to journals and the media. Two of the major research teams make a point of rejecting the taint of National Geographic and its film crews. In counterpoint, the book repeatedly notes the long association between National Geographic and the Leakey family, including a direct contrast between the histories of Richard and Maeve Leakey and Tim White. Amid descriptions of media-savvy scientists, we see Henry Gee, editor of Nature, commenting on fossils, prognosticating on future discoveries, "prodding" researchers, and having one incredible meeting that was hard for me to believe even after reading it. If one wonders about possible conflicts of interest for Gibbons, how much more must one wonder about the chance of one of these papers being rejected by Nature's vaunted six "peer reviews"?

At its bottom line, the book really raises two substantive issues. The first is the real danger of today's field work. Paleoanthropology is not merely a game today, it is "the Great Game" replayed. Field teams divide up "Connecticut-sized" research territories, hem opponents into areas with younger sediments, and -- when bullying, scientific name-calling, and bureaucratic manouvers fail -- finally agitate local people, enlist bandits, or pull their guns. To me, the book's most touching moment is its description of Michel Brunet's feelings after losing a colleague on his field team. In another episode, a young graduate student (who deserves recognition for her science and not this) personifies a near-miss with violence in the field. The two cases together bear rereading: if paleoanthropology continues along its current path, then who can doubt that some people will be killed in the field?

The other issue is the relationship between these field teams and the science as a whole. As depicted in the book, they clearly do resemble explorers looking for the source of the Nile. They know what the goal is -- at one point, Pilbeam even sketches what the ancestor will look like, at another Henry Gee opines about it. It is still out there waiting to be found, and these teams will be searching until they find it. It's "the First Human" of the title.

But these fossils aren't human -- and it's darned hard to tell whether they are even the more humanlike kind of apes! In the book, we see that the science turns against the scientists sometimes. Ramapithecus is no longer considered hominid by anybody -- it's not even a valid taxon anymore. Louis Leakey's Kenyapithecus wasn't a hominid either.

Can it be that all of these new fossils are really hominids? Or have some of these scientists in their quest for older and older fossils overshot the mark? The current scientific debate over specimens is only glossed here -- the book sketches what the disagreements are, but gives no details to judge the arguments. (If you want those details, you'll need to read the blog!) Instead, the science appears as another forum for the scientists to misbehave -- accusing each other of holding "creationist positions" and the like.

Many readers will surely be puzzled to read how these men and women, who brave disease, bullets, broken families and years of denial, can be so poorly composed in the face of scientific examination. Again and again we see them squirrel the fossils away, withdraw them from the world, or give up on paleoanthropology altogether. How can it be that this story is repeated so many times? But the reader should consider: No one can take away Hillary and Norgay's summit photos. But even after all the years of work, the lowliest graduate student might turn one of these "hominids" into an ape.

Even I make a brief appearance in this book -- blink and you'll miss me dancing through to aggravate Brunet's heart condition.

And it comes from me! My paper with Milford Wolpoff, Brigitte Senut, Martin Pickford, and Jim Ahern is now available online from PaleoAnthropology! The PDF is freely accessible -- a big advantage with this journal. So go download!

Here's the abstract:

The Toumaï cranium TM 266 is the first known from any Late Miocene African hominoid clade, and is one of the best preserved crania of any Miocene hominoid. Since its publication there has been debate in the scientific literature and discussion in the popular press over the assertion that this cranium is significant because it is the earliest known hominid. The basis of the hominid assessment rests on two interpretations of the anatomy: a hominid-like, small, flat-wearing canine; and, cranial features reflecting an upright stance and bipedal locomotion. In fact, it is widely reported that the specimen is an upright hominid biped (Haile-Selassie et al., 2004; Kimbel, 2004; Lieberman, 2002), although this is yet to be verified by independent observations and study. The history of paleoanthropology may be relevant to this assessment, because there have been similar claims for other extinct primate species. Here, we evaluate the hypothesis that Sahelanthropus (the genus TM 266 is attributed to) is a hominid by examining features of the canine and of the cranial base that are said to reflect canine reduction and change of function, and upright posture and bipedal locomotion. These are hominid autapomorphies and their presence or absence in late Miocene hominoids has fundamental importance for identifying the hominid clade (Wolpoff et al. 2006:36).

There are two important differences between our analysis and earlier analyses of the skull. First, we provide more comparative data from Miocene primates. Some of the apparent similarities with hominids -- especially considering the morphology, size, and wear on the canines -- are clearly present in other Miocene ape lineages. This is of course the primary difficulty in defining hominids on dental remains alone, since several lineages of Miocene apes appear to have been convergent on some hominid dental features. These similarities don't preclude Sahelanthropus as a hominid, but they remove a major support for that hypothesis.

And second, we provide a biomechanical assessment of the reconstructed skull and its relevance for bipedality and posture. Rather than simply looking for similarities with hominids or chimpanzees, we actually developed a model for how the skull and neck musculature must have functioned. One angle in reconstruction makes the skull look like modern humans -- the foramen magnum - orbital plane angle. But regardless of this angle, the skull actually cannot have functioned in a vertical posture because of the length of the nuchal plane and vertical height of inion. Also, this angle in Toumaï doesn't look anything like early hominids -- australopithecine skulls have FMOP angles similar to chimpanzees!

I think this line captures the point:

The point is not that the TM 266 cranial rear and posterior portion of the cranial base was unlike hominids because the region looks like apes, but that TM 266 had a posture that is not upright because the region reflects nuchal functions similar to those of apes (Wolpoff et al. 2006:46).

There's lots of other interesting stuff in the paper also -- including a section about the hominid-chimpanzee divergence date that I never thought we would say, but is looking very prescient considering recent data. It was a real pleasure to explore several different topics and bring them together, and we'll have much more to do!

References:

Wolpoff MH, Hawks J, Senut B, Pickford M, Ahern J. 2006. An ape or the ape: is the Toumaï TM 266 cranium a hominid? PaleoAnthropology 2006:36-50.

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

A concise 4-paragraph article by Mathieu Schuster and colleagues reports on dune deposits that show the Sahara formed during the Late Miocene.

After the mid-Holocene humid period (6000 years ago), arid conditions developed throughout North Africa, culminating in the formation of the Sahara, which is the largest warm-climate desert on Earth (9,000,000 km2). However, earlier desert recurrences in the region are also documented. Direct evidence for eolian deposition is given by thermoluminescence dating for the Late Pleistocene; e.g., in Mauritania [25 to 15 thousand years ago (ka)] (1) or in Tunisia (86 ka) (2). The latter is currently considered as the oldest terrestrial record for desert conditions in the Sahara (2), even if firm evidence exists for a pre-Quaternary Great Western Sand Sea in Algeria (3). Some earlier arid episodes (Miocene-Pliocene) were also suggested by marine records off West Africa (4); but until now, no contemporary in situ eolian deposits were known in the Sahara region. In the northern Chad Basin, we recently identified and dated widespread outcrops of eolian dune deposits that are distributed over an area more than 2000 km². Our results testify that the onset of recurrent desert conditions in the Sahara started at least 7 million years ago (5-7) (Schuster et al. 2006:821).

The desert comes and goes, expanding and contracting -- and those vacillations are recorded by this earliest evidence, also:

In the Toros Menalla region, these eolian sandstones are conformably overlain by a horizon bearing abundant vertebrates fossils, including Sahelanthropus tchadensis, the earliest known Hominid [sic] (5, 7). In this horizon, named the Anthracotheriid Unit, biostratigraphic correlation of the mammalian fauna indicates an age of 7 Ma (5–7).

Now, this isn't news (which I'm sure Science didn't bother to check) since Vignaud and colleagues (2002) published the same evidence, complete with the wind direction chart:

The lower part of the section (at least 4 m thick) is composed of fine to very fine white sands, poorly cemented, and is mainly constituted by numerous quartz grains, without matrix. The grains are well sorted, well rounded, matt and frosted, and are strong evidence for aeolian modelling. The foreset laminations (avalanche laminations in front of the aeolian dune) represent a typically aeolian deposit. These sands show cross-beddings that progressively decrease in size from the bottom (1 - 2 m) to the top (20 cm). This facies exhibits typical alternations of grain-fall and grain-flow laminations, characteristic of aeolian dune deposits. Our interpretation is confirmed by frequent wind ripples at the foot of the fossil dunes, whose crests are perpendicular to the direction of dune progradation. These fossil dunes are, to our knowledge, the oldest evidence for desert conditions in the southern Sahara area (Vignaud et al. 2002:152).

I guess this is the science journal equivalent of getting "punk'd" -- "Ha ha! You published what we printed four years ago!"

I opened up the Vignaud paper to double-check the paleoenvironment in the fossil-bearing layer. From the faunal list, they conclude this:

The oldest known East African hominids (Ororrin [sic], Ardipithecus) are contemporary with faunas associated with wooded environments. Younger australopithecines lived in a wider range of habitats. In contrast, the TM 266 vertebrate fauna contemporary of the Toros-Menalla hominid suggests a mosaic of environments from gallery forest at the edge of a lake area to a dominance of large savannah and grassland. Determining the precise habitat of the TM 266 hominid locality among the mosaic of environments available to it constitutes a research challenge to be met by further laboratory and field studies currently in progress (Vignaud et al. 2002:155).

They (Vignaud et al. 2002) interpreted the succession of dune and lacustrine deposits to mean that the hominids lived in a mosaic environment near sandy desert, but locally including marshy/swampy, lake, and gallery forest. An alternative interpretation might be that the desert really receded (or disappeared) during the later time period when the hominids were there. In either case, the paleoenvironment is interesting, because it means that the Sahelanthropus-like primates colonized (and possibly repeatedly recolonized) areas that were periodically dune desert (and therefore probably not habitable by large primates). This may not mean much in terms of locomotion -- the hominid-bearing unit is clearly water-rich, and we can't refute the idea that the surroundings were as woodland-like as those preserved in the Late Miocene Middle Awash localities.

But I think it is a good hypothesis that all of these apes (or hominids) were very cosmopolitan compared to extant chimpanzees and gorillas. The question is whether their actual dispersal abilities were different from chimpanzees. Prehistorically, genetics would seem to indicate that chimpanzees had long-distance dispersal; the only fossil evidence of chimpanzees has been found in a region that historically did not support chimpanzees; and they today successfully utilize relatively open savanna at the eastern end of their range.

So it is by no means obvious that the cosmopolitan nature of these Late Miocene lineages would have required a specialized terrestrial adaptation -- at least not beyond the specialization of knuckle-walking. So why become bipeds?

References:

Schuster M et al. 2006. The age of the Sahara Desert. Science 311:821. Full text (subscription)

Vignaud P et al. 2002. Geology and paleontology of the Upper Miocene Toros-Menalla hominid locality, Chad. Full text (subscription)

The weblog didn't start from zero a year ago; the sections related to my courses and the Flores files long predate that. But it has been a year since I started daily updates and regular reviews. It has been a great year here, with an immense growth in readership -- December ended with over 1500 daily readers. I want to give my thanks to everyone who has helped, by reading, contributing ideas, or sending papers. Please keep it up!

In the coming year, you'll be seeing more of my writing elsewhere, in addition to some very interesting (and long-awaited) research papers of my own that will be coming out. It should be a year of great announcements, and maybe a few discoveries.

So I think in lieu of a look back over last year, it would be appropriate to start 2006 off with some predictions. Here is a list of my top ten predictions for 2006, ordered from most certain to most speculative. As with most predictions, I've tried to keep an appropriately Delphic tone. And I've excluded almost everything related directly to my own work, which makes the predictions more fair, but leaves a couple of fairly obvious gaps.

• 10. We will see a name for the Flores pathology.
• 9. There will be two Neandertal genome-related announcements.
• 8. No Ardipithecus.
• 7. "Population cluster" will become the new "race".
• 6. There will be another paper (yes, besides the one last month) using genetics to estimate the time of the human-chimpanzee divergence. The date will be 5 million to 7 million years ago.
• 5. Evidence of recent selection will be found for several Y chromosome genes.
• 4. Sahelanthropus postcrania will be published.
• 3. There will be an ancient DNA announcement from China.
• 2. StW 573 will be proposed as a new species ancestral to all later hominids.
• 1. A Hawks weblog post will be cited in a peer-reviewed research paper.
• BONUS: A new Georgian hominid will be a robust australopithecine.

This month's Discover came in the mail today. In celebration of their 25th anniversary, their issue is devoted to "Frontiers of Science", with articles covering the (speculated) cutting edge in different fields. One spread is dedicated to "Human Origins", with a short piece by Carl Zimmer, an interview of Tim White, and a graphic.

Zimmer's article, "Digital ancestors walk again" covers the increasing use of CT imaging and reconstruction of hominid fossils. The subtext is that anything high tech must be better -- for example, the article labors under the misimpression that we cannot study endocranial contours without cutting a skull open.

Also, a read of the article gives the impression that every finding from this new advanced technology supports splitting hominids into several species (in particular, it mentions the Liang Bua endocast reconstruction and the virtual Neandertal growth series assembled by Ponce de Leon and colleagues). Probably this trend will continue as long as few people work with scans except the people who do them.

Here's the conclusion:

As the use of CT scans expands, paleoanthropologists are developing new avenues for uncovering clues to our past. They are discovering signs of healed wounds, of toothless old hominids who must have been cared for by others. Some researchers are even producing full-length virtual skeletons to which they can attach virtual muscles and make the ancient hominids walk again. Most significantly, CT scans can liberate hominid fossils from museum drawers. Once a research team makes a scan, they can post the data on a Web site for other researchers to analyze, bringing a precious hominid fossil to new sets of eyes and new sets of questions.

So utopian....

But Tim White has a different view of the kind of technology changing the field:

What technology advances are changing the way you study evolution?

W: The global positioning satellite system. WIth GPS, we no longer have to worry about the position of a fossil. Some of the biggest blunders in the history of paleoanthropology were made by people who lost the place where a fossil came from. There's no excuse for that anymore. The other big advance is in geochemical dating....

No CT scans there.

Personally, I think CT will have a limited set of impacts. The best thing is that it will allow any lab in the world to have as full a set of comparative data as have been released. Currently, it's useless for that purpose; there's just not enough access. But that is changing, and CT scans are as useful to a practiced eye as casts -- which are much less available today even as CT increases. In fact, high-resolution CT may essentially end casting of new fossils, since that is one of the major sources of damage. We'll be doing a lot of comparative work with imaging in the future.

On the other hand, I think CT will have a really limited impact on the study of new fossils. For one thing, those of us who are used to studying fossils are trained to deal with fragments. People do reconstruct fossils, but reconstruction is not essential to studying most morphology. Another thing we are trained to deal with is distortion. Especially plastic deformation can affect the very shape of the fossils we work with. We correct for it by examining which morphology is affected or unaffected, and by making conservative estimates. CT imaging is too tempting in this scenario -- it encourages people to think they have corrected problems, when instead it is merely adding geometric assumptions.

CT imaging and reconstruction is often proposed as a way to deal with distortion and fragmentation: Zimmer mentions the "sophisticated mathematical software to find the best way to assemble" reconstructions. But these can end up just as biased as any handmade reconstruction, even when the distortions are fairly apparent. There has been substantial disagreement about the CT reconstruction of Stw 505; we may find that the reconstruction of the Sahelanthropus skull faces similar problems.

There are three main benefits of CT reconstruction: it allows repeated trial and error assembly without actually grinding bone contacts against each other, it allows mirror-image substitution for missing parts, and it allows a skull to be geometrically fit to a model. The repeated trials are very valuable: they give an experienced anatomist a chance to try slightly different configurations to sense the range of variation resulting from the state of preservation. The mirror-image reconstruction is valuable for visualization, but potentially misleading for scientific comparison -- try taking a flat mirror and reflecting half your face: notice how hard it is to align the mirror properly and how odd it makes you look and you'll have an impression of the problem. The widespread use of geometric fitting is a potential disaster: by encouraging the use of a model, it reduces the range of biological variability expressed in fossils. When these mathematically-fitted reconstructions are then fed into mathematical comparisons, the structure of the data will be biased by the reconstruction technique in ways that may not be visually apparent.

Anyway, despite all the math, the computer is only as good as the scientist running it -- the principle of "garbage in, garbage out" is everlasting.

Discover magazine has been doing a series of retrospectives by scientists on the last 25 years of progress in science, in honor of the magazine's 25th anniversary. The current (July 2005) issue has paleontologists discussing what, in their views, were the most important finds of the last 25 years, and what they expect to be the most important of the next 25. Included in the group are several paleoanthropologists. Here are some snippets:

Richard Leakey:

The most important event in paleoanthropology during the past 25 years is the discovery of a fossil skull, 7 million years old, of an anthropoid that has been named Sahelanthropus tchadensis. The anatomy of this specimen forces a debate on what is most fundamental: What, if anything, distinguishes an early ape from an early hominid?

Chris Stringer:

The most important development was the coalescence of fossil and genetic data to show that our species had a recent origin in only one region -- Africa -- and that everyone traces their origin back to that continent. Regional differences lie in only a few genes that evolved during the last 100,000 years, as humans spread out and settled the areas where we find them today.

Christopher Beard:

During the last 25 years, the greatest advances in primate paleontology have been in charting the very beginnings of the anthropoid radiation . . . . My colleagues and I found the first of these dawn monkeys, which we named Eosimias sinensis, in China.

Richard Klein:

Archaeological and especially genetic advances over the next 25 years should clarify whether the modern human expansion was grounded in a quantum behavioral (cultural) advance, and if so, whether the advance stemmed from a genetic change that fostered the modern human brain.

My favorite is Tim White's response, partly because it generalizes more widely than the others, and partly because it is the change that underlies my efforts here:

I think that the most important development in paleobiology during the last 25 years was the networking of paleontologists and colleagues via the Internet. When paleontologists discovered that they could communicate quickly and economically across global distances, collaborations blossomed and intensified.

Of course, I wouldn't say, as he goes on to imply, that internet collaboration led to new discoveries of Ardipithecus....

The picks from non-anthro paleontologists are likewise a mix of entertaining and enlightening, with Mark Norell and Kevin Padian both citing the Liaoning fossils, while Jack Horner chose the recent T. rex soft tissue discovery, and many others were represented as well. In all, a chance for a little self-promotion and a mix of topics with some obvious predictions and some more interesting ones.

Mark Weiss from NSF appeared at the AAPA business meeting to discuss recent changes in the funding guidelines from the Physical Anthropology program. The most significant change, effective in the upcoming (July 2005) funding cycle, is the requirement to file and follow a data access plan with every grant. This change is the NSF response to the questionaire circulated last year among physical anthropologists and archaeologists. It follows policy changes at the top levels of NSF, ultimately initiated by the Clinton and Bush administrations toward greater openness of publicly funded research data and protocols.

From the Physical Anthropology grant information page:

NSF is committed to the principle that research supported with public funds should be made widely available. Under NSF's data sharing policy, the Foundation expects investigators to share with other researchers, at no more than incremental cost and within a reasonable time, the data, samples, physical collections, and other supporting materials created or gathered in the course of the work. To implement that policy in ways appropriate to Physical Anthropology and Archaeology, beginning July 1, 2005 these Programs will require that all proposals include a one-page detailed description of the applicant's data access plan in the "Supplementary Documents" section. This page will be in addition to the standard 15-page project description. Applications lacking this statement will not be reviewed. The Programs realize that individual cases may differ widely and recognize that any absolute timeline or rigid set of rules is not possible. They also recognize that revision and adjustment may often be required as the work proceeds. The data access plan, however, will be considered an integral part of the project and therefore subject to reviewer and panel evaluation. Major departure from it will constitute a significant project change and require NSF approval. Successful applicants will be required to address this issue in every progress and final report. PIs on all awards made under these guidelines will be expected to discuss implementation of their plans in the "Results of Prior Research" section when they submit subsequent applications.

To me, this appears to be a good compromise between the different positions on data access. Some researchers would prefer to have casts, photographs, and measurements of specimens become publicly available (without restrictions) immediately after they are published. Others (including a subset of primary excavators) would prefer to limit access to photos and data until after a full monographic treatment of the specimens is published. There are good arguments on both sides.

In favor of limiting access, specimens are rare and fragile, and access to them should be carefully limited to preserve them. The skills required to prepare fossil specimens are rare, and they must be cultivated in long-term research projects. The only way that such projects can survive is if they can maximize the impact of their most important finds, and this means controlling the publication of pictures, limiting the creation and distribution of casts, and promoting students of the principal invesigators as groundbreakers making new and important discoveries. If such research projects had to make their data public immediately, there would be no incentive for them to continue their work.

But even those who are in favor of limiting access to fossil specimens must recognize that the situation in paleoanthropology today does not benefit them. There are very few publicly accessible datasets. Even pure electronic data for which analysis has been published and for which the cost of transmission is negligible, such as CT data, generally cannot be had. There are exceptions, who either provide data for sale or for free, and from the bottom of my heart I thank them for their choice to better the science. Their choice is all the more laudable, because the situation at present has created absolute disincentives to share data. At present, closing access is the only way to punish freeriders who fail to share data themselves. And commoditizing data and casts can be the only way to get valuable data out of other researchers.

And in my opinion, the issue of access to new fossil hominids has received an unwarranted share of the attention. Ann Gibbons' 2002 article, "Glasnost for hominids," is an excellent treatment, but it only scratches the periosteum of the problem. If the only problem with access to specimens was that only a few people could see something until ten years after it was unearthed, that would be bad, but still much better than the situation as it stands.

The real problem is that twenty to thirty years after many fossils are uncovered, there is no cast availability, little public data access, few financial accommodations to make such access possible. Specialists like me often find ways around these barriers. But I do not think it would be overstating the problem to suggest that perhaps half the people teaching human evolution in four-year universities have never touched a cast of a Hadar fossil. I would be delighted to be proved wrong, but I don't think I am. Our field is educating students into a world in which A. afarensis is unknown in the laboratory and poorly represented in our textbooks. I'm not talking about new specimens, here, I'm talking about fossils that were found in the mid-1970's and monographed in 1982. Nor is this problem limited to early hominids. What proportion of people teaching about the modern human origins problem do you suppose have seen a cast of any "early modern" fossil other than Skhul 5?

One may object that this kind of teaching effort really isn't the same thing as primary research, and one would be right. But I am one who thinks that teaching is essential to my research. And I see it the same way as my high school band teacher: you can't have a good high school band without a good junior high and grade school band program. We can't train competent professionals without a strong undergraduate training, and the undergraduate training of our professional paleoanthropologists is a lot more varied than the graduate programs. Unless we strengthen the broad base of the field, we have little hope of strengthening its research depth.

And the fact is that primary paleoanthropological research is no longer the province of a few dozen professionals. The field is increasingly interdisciplinary, involving hundreds of people with no expertise in anatomy at all. The fossil record is an afterthought to many of these people, and it is our task to continue to show its relevance. We can't do this without the tools.

Righting the paleoanthropology ecosystem

In this sense, the current ecosystem in paleoanthropology is dysfunctional, and the problem of data access has had a negative impact on the quality of science in the field.

New specimens are a bottleneck in paleoanthropological research. The pace of research is positively limited by the rarity of fossils. This bottleneck has several consequences, including the complete absence of research on some topics that are poorly addressed by fossils, the high citation rates of initial announcements of fossil discoveries, and a funding structure that privileges field research leading to new discoveries. Because this bottleneck is so acute, a naive observer may confuse it for the entire field.

But except for this one part, paleoanthropology as a whole is a normal part of evolutionary biology. Like other parts of biology, ours is a comparative science in which all competent work depends on thorough procedural knowledge of evolutionary theory and factual knowledge of comparative samples, such as extant apes, humans, and other primates.

Even most paleoanthropologists do not themselves recognize the breadth of their field. There is a tendency to see the field as an unstable ecosystem, in which a very small number of primary producers (who find new sites and excavate and prepare fossils) support a huge number of consumers:

The classical ecological pyramid has a broad base of primary produces, with increasingly smaller numbers of secondary and tertiary consumers. Modern paleoanthropology, however, is like an inverted ecological pyramid. Armchair commentators abound. Actual producers of fossil data are increasingly rare. But boosting the number of producers is not feasible because so few professionals have the requisite specialized skills. Even fewer are qualified to teach them. The production of primary paleoanthropological data requires physical search, discovery, extraction, dating, contextualizing, preparation, photography, molding, analysis, writeup, and publication. The process now takes years of work by large coordinated teams (White 2000:289).

Tim White is one of the premier fieldworkers in the discipline, and it is not surprising that he should display a fossil-centric view of the field. But is it really true that we have nothing of value besides the fossils; that they are the only "product" we deal in? Are the rest of us really nothing more than jackals nipping at his heels?

I would propose an alternative model of our ecosystem. Rather than privileging the mere objects that fossils actually are, I would privilege the knowledge that we gain about human origins from them. Fossils are far from the only source of this knowledge. Indeed, all the knowledge that we obtain from fossils ultimately comes from comparing those ancient fragmentary remains with the more complete comparative samples of extant species, not to mention their rich genetic, behavioral, and soft-tissue morphological record. Even modelers and mathematicians, like myself, wring data out of fossils that ultimately do not inhere in the bones themselves but in their relationship with other specimens and species.

Left to itself, this work is steady and vegetative. We produce observations, comparisons, hypotheses, and ultimately evolutionary theory. We travel, we study specimens, we present our work to public audiences and to groups of our peers for scrutiny and comment. And this open process helps us to make our knowledge better. Without a single fossil, this body of theory would be left sorely wanting for accuracy, but it would exist nonetheless and would be nonetheless be the most valuable evidence for our evolution that we have. Just as Darwin's Descent of Man preceded all but the Neandertals, our work today precedes the next hundred years of fossil discoveries and awaits testing in light of them.

Those of us familiar with this kind of work tend to call it not "armchair commentating" but instead "critical thinking." We train our students in it, and work to make them knowledge producers as well. We socialize them that the best way to succeed in the real world is to share data and to play well with others. And we hope they won't get burned in their first encounter with a real predator.

Our field has its T. rex and the like. The activity of these top predators is spastic and episodic. When they roar, presenting us with a new precious relic, much of the field cowers and prays that we don't have to relearn everything from our graduate training that the new fossil makes obsolete. These carnivores devour comparative biology, for their fossils have little relevance outside its context. Newton called it "standing on the shoulders of giants," but sometimes it seems more like Spinal Tap dwarves trodding on a tiny Stonehenge.

Most of us recognize that new fossils are more than bludgeons to beat away the jackals. They are the only tests that many of our hypotheses can ever hope to have. And I don't see anything to be gained in classing part of our science as highly important and another part as irrelevant or worse. The fact is that all of us work with each other's data and conclusions. Some of us have established barriers to make that process more difficult. All of us deal with the same bottleneck of fossil evidence, but for many of us that bottleneck is a mere inconvenience, while for others it is the crook used to lever an entire career.

It is fitting and just that the acquisition of new fossils should be a high funding priority; if not the highest. This bottleneck prevents progress, and we should do anything in our power to alleviate it. But high funding for new field research does not imply that access should not be more open.

Closed access unnecessarily impedes progress in other areas that might otherwise be made. The present situation is unstable, and I see these critical problems:

1. The slow reporting of specimens and failure to share casts and data slows research on some important topics, limiting them to a small cadre of researchers. As an extreme example, no study of the energetics of the earliest bipeds is now possible, because many major specimens currently exist without having been reported, and none of the people working on them specialize in energetics. But more practically, only two years ago it was reported that only a single person had seen all of the then-extant evidence for Miocene hominids (Gibbons 2002). How can a field progress when so few people are in a position to review its data? If these people review each other's papers (because they are the only recognized experts), then how can any of us have confidence in their rigor?
2. Studies published on inaccessible fossils are not replicable. Suppose that someone publishes the energetics of the earliest bipeds, using measurements from new specimens. Certainly anyone reading this research can run the same measurements through the equations, but how can they be sure that the measurements are accurate or relevant, without examining the fossils or reconstructions themselves? This is the current situation with Sahelanthropus and its CT reconstruction, for instance: the publication exists, but is not replicable because access does not exist.
3. Students who can study inaccessible fossils can trade on this knowledge to promote themselves. Now, I don't think there's anything wrong with self-promotion; after all, jobs are scarce. But quality of access has increasingly become confused with quality of training. Ideally, a student will have both. Paleoanthropology is a comparative science, and extensive experience with comparative samples such as extant apes is needed for any competent research. To the extent that some students exploit the fossil bottleneck to leverage greater visibility, the quality of training expected of new hires is diminished.
4. Casts are generally inaccessible. Despite the current ubiquity of CT scanning of fossils and creation of stereolith casts, even these cannot be purchased. All of the problems above would be less pressing if there were some assurance that eventually all qualified researchers would have access to casts and scans. But when an initial description, peer-reviewed by only friendly colleagues, stands for decades without reanalysis because of the lack of access, a mistake that shouldn't occupy more than five pages in a dissertation ultimately bends the course of the discipline for years.
5. Most important, public support for our discipline depends on its perception in a country where a majority of people don't believe that humans evolved. Those arrayed against us argue that new fossils are hidden away and not studied by the scientific process of peer review. They argue that many human fossils are manufactured, and that there are no guarantees that they are not the product of a small group of scientists with an anti-creationist agenda. As long as we do not open access to the primary evidence of human evolution, these criticisms are not only damaging, as far as the nonspecialist public is concerned they are also valid. We do nothing but damage the profession when we fail to share the products of our research as freely as possible, not only with each other, but with humanity.

Will the policy work?

To the extent that new grants will make data more available, will encourage the spread of CT scans of fossils, and will help to spread photos and observations of new discoveries to the public, I think the data access policy will be helpful. I think there may be nothing to be done about the availability of casts, as long as museums control their reproduction. I respect and value the work of all museums who conserve fossil remains, but they are not set up for widespread public sale of fossil replicas. And a commercial solution will have little incentive to reproduce rare fossils that are not part of the central story of evolution. In my opinion, the most important aspect of data access is to increase the effectiveness of peer review and to guarantee replicability of research. For these goals, I think the new policy has a maximal chance of success.

Of course the real test of the value of the new policy is to see whether grants start to be declined on the basis of data access restrictions. As I read it, this new policy basically sets the clock at zero. There is no condition that specifies that previously funded work should be made public, and no effective means of pressure to create a situation favoring the sharing of old data and specimens. There are now specimens that have been out of the ground for thirty years that cannot be studied. There are hominid specimens that have been out of the ground for ten years or longer that remain undescribed. This situation will not change.

If the new policy is to be a success, then the proof of it cannot wait for ten to thirty years. It needs teeth. It needs two or three high-profile grants to be declined because of data access issues. And it needs those cases to be made public, so that everyone can have confidence in the openness of the process. This doesn't mean that the names of the applicants and their alleged sharing violations should be dragged through the press. It does mean that NSF should publish the number of grants (and their proposed funding amounts) declined for failings in the data access plan.

But more importantly, it needs replication among other granting agencies. A large set of molecular anthropologists have just shown their willingness to completely forego public funding, in order to maintain certain kinds of controls (in this case ethical ones) over their research (See Genographic Project). Will paleoanthropologists do the same? It would be helpful if some of the important private foundations, such as the National Geographic Society, the Leakey Foundation, Wenner-Gren, and others would establish data access provisions also.

Another helpful idea would be for one of these foundations to establish a data bank. Notice what is missing in the NSF policy is any discussion of a data archive. Other areas of NSF and NIH have such archives and maintain policies of mandatory deposition of data. This is most prominent for genetics, with the GenBank archive and journal publication of most results conditional on mandatory submission of data to the archive. Thus, there is no logical impediment to the creation of such a resource by a federal agency. The fact that they chose not to implement such a policy, I find significant.

Among other considerations, this choice probably depended upon discussions with museums and governmental agencies in other countries, who are the conservators and permit-granters for most fossil research. There are good reasons for the U.S. government not to compromise the activities of international museums by making public images, casts, and CT data of their fossils. On the other hand, much money and effort could be saved if such an archive were available, and it would increase the quality of published science by increasing sample sizes, consistency of measurements and estimates. It would also help conserve the fossils by protecting them from the investigators themselves. Non-governmental agencies are probably the best sources for such a centralized archive because they may have more ability to work directly with multinational sources to broker a solution. In my opinion, such an archive would be more important and would have a more positive scientific effect than five years of ordinary research funding for such an organization.

Not so long ago, Wenner-Gren was the principal international sponsor of cast production. There is no logical reason why it or some other foundation could not be again.

Final thoughts

This turned into more of an essay than I really intended, but it is a subject that I think all of us are strongly invested in. The issues at stake are what kind of science we want to have, and how do we want to limit access to its findings. I believe that our research should be as public as possible. I think that openness leads to better science, and I think that restrictions to access only make us suffer at the hands of those who wish us ill. I hope that this new policy will lead to more conversations about the future of the field. I will be most pleased if I can play some role in moving those conversations forward.

References:

Gibbons A. 2002. Glasnost for hominids: seeking access to fossils. Science 297:1464-1468.

White TD. 2000. A view on the science: physical anthropology at the millennium. Am J Phys Anthropol 113:287-292.

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.

The April issue of Discover has a feature article on PhyloCode, focusing on the roles of Jacques Gauthier and Kevin de Queiroz in trying to revise the code of biological nomenclature. It is an interesting introduction to the issues, but is a little short on specifics, so I went to some additional resources to examine the impact of the whole PhyloCode debate on human phylogenetics.

Proliferating ranks

PhyloCode is an attempt to address two simple problems with the Linnaean system. The first is the problem of ranks. The Linnaean system provides seven ranked positions for species and higher-order taxa. These are the levels familiar to anyone who can remember King Phillip's soup, or his Peter's German origin, or any of the other mnemonics. These seven levels (kingdom, phylum, class, order, family, genus, species) have been supplemented over the years with in-between levels at almost every rank, such as suborders and infraclasses. For example, the most basic division among living primates is into superfamilies, which is the rank occupied by hominoids (great apes and humans), cercopithecoids (Old World monkeys) and ceboids (New World monkeys). The grouping of all three of these superfamilies, Anthropoidea, is a suborder, while the grouping of Old World monkeys and hominoids is the infraorder Catarrhini.

But when it gets to the level of infraorders and superfamilies, the phylogenetic pattern of relationships is already stretching the Linnaean classification to its limits. This degree of differentiation is more or less well suited to primates, but many other groups of organisms have even more complicated phylogenies with many more branches. This leads to some big confusion:

As part of their work, [Gauthier and de Queiroz] created a lizard family tree, but when they began to assign names to the important branching points on the tree, they realized there were more groups to name than there were ranks in the traditional system. "I started using these exotic ranks like parvorder, cohort, and microorder, and all that kind of crap," Gauthier says. "Then we'd learn more about the tree, and all the names would have to change. I thought, 'That sucks. All these ranks, they're a problem.'" (Foer 2005:48-49)

This is a problem I've thought about for a while also, ever since I was learning Mesozoic mammals and encountered exotic taxonomic ranks like "tribe" and "domain." Unlike suborder and infraorder, many of these give no indication at all about where they belong in the phylogenetic hierarchy. If this complication actually helped organize species, that would be forgivable. But even the extension to thirty or more ranks is not enough to encompass all the possible groupings in some phylogenies, especially where extinct species must be placed in a hierarchy including living species and their ancestors.

And of course the probability of disagreement among authorities on names increases combinatorially with more taxonomic ranks. Even within the hominoids there is at present substantial disagreement on the names of groups at almost every taxonomic level, despite the fact that almost everyone agrees about the phylogeny of the living species of apes and humans. Some of this disagreement is purely nomenclatural, while the rest comes from genuine disagreements about the phylogeny of extinct apes. It seems especially problematic that disputes about the relationships of extinct and fragmentary fossils could substantially alter our judgment about the nomenclature to apply to living species, but that is exactly where we stand.

Hominids and hominins

This leads to the second major problem of the Linnaean system, the problem that the names of groups themselves are formulated in a way that cannot be divorced from their taxonomic level. What this means is that if our hypothesis of phylogeny changes, the names of taxa must also change. The problem with this is that it subverts the goal of communication:

In the zoological code, family names must end with the four letters idae, for example, and subfamily names must end in inae. If taxonomists decide that a group once considered a family should instead be ranked as a subfamily, the group must, under the rules of the current system, get a new name. This frustrates the PhyloCoders to no end. "It's still the same tree," Gauthier says. "Nothing has changed, except how we spell the names. In a day when all this information is going onto the Internet, this is a bad idea. It's a constant change of PIN numbers." Some taxa have gone through a number of different names over the course of just a decade. Several years ago, for instance, it was decided that the great-ape family Pongidae couldn't exist at the same rank as the human family Hominidae because humans are a subset of the great apes. To fix the problem, researchers proposed that humans and their great-ape relatives be combined into a single family, Hominidae, and members fo the family Pongidae became the subfamily Ponginae. This can make literature searches a real pain, Gauthier says: "To a computer, there is a world of difference between iguanidae and iguaninae" (Foer 2005:50).

In my mind, computers are the least of the problem. Replace "to a computer" with "to an undergraduate" and you are closer. Really, even this understates the problem. If we could ensure that a new taxonomy established by universal consensus today would not change in the future, then it would be well worth changing all the names. But we can be pretty sure that things will change in the future, repeatedly. It just isn't worth having a system where the names have to be changed all the time, because such changes render all past research at best confusing, or at worst nonsensical.

The Hominidae-Homininae problem is not the only one in paleoanthropology, but it is a convenient example. Foer's description of the problem is one possible reformulation, but not the most popular one. We all recognize that African apes and humans are more closely related than either is to orangutans, and chimpanzees and humans closer than either is to gorillas. Many people would apply Hominidae to all the great apes, ponginae to orangutans, and homininae to the African apes and humans. This leaves the human lineage (including australopithecines) in the "tribe" Hominini (The tribe Panini would therefore include tasty Italian bushmeat sandwiches). Thus, orangutans would be hominids, gorillas would be hominines, and australopithecines would be hominins.

Consider the problems with this arrangement. First, it isn't comprehensive. There is no name for the human-chimpanzee clade, for example. The taxonomic level for that clade would properly depend on the details of the evolutionary divergence among gorillas, chimpanzees, and humans. If, for instance, there was a substantial adaptive radiation between the gorilla divergence and the human-chimpanzee divergence, then these fossil lineages might be placed with chimpanzees and humans within an infrafamily, with the chimpanzee-human clade placed as a supertribe. Likewise, the branch points leading to the dryopithecines depend on their relationships with the later African apes, or even to the Asian apes. In other words, the taxonomy still hangs on currently unknown phylogenetic branchings, and the choice of taxonomic level is entirely arbitrary.

The arbitrariness of the naming system is highlighted by some other alternatives for the hominoids. For many years, molecular researchers like Morris Goodman have suggested that the genetic similarities between chimpanzees and humans are consistent with those within genera of most mammals, and the time of origin of these lineages is also consistent with the antiquity of mammalian genera. So Goodman et al. (1998) took the logical step of including both humans and chimpanzees in Homo. The great apes in this scheme are all hominins (tribe Hominini) and the living hominoids are all hominines (subfamily Homininae).

By discarding past consensus, arbitrary changes impose a cost on any researcher or student, in discarding past consensus. The past fifty years or more of paleoanthropological research have shared a clear meaning for the term "hominid." Of course, one may read that literature today while remembering the past meaning of "hominid," just as we remember what "pithecanthropine" used to mean. But it is a cost that should come at some benefit. For "pithecanthropine," the loss of the genus Pithecanthropus combined with the discarding of the idea of a "pithecanthropine stage" of human evolution means that we no longer have any call to use the term. The benefit of the change is simplification and the recognition that an incorrect hypothesis of evolution has been refuted.

Many would argue that the replacement of hominid with hominin has similar benefits. After all, the use of "hominid" in the past was partly conditional on the acceptance of the family Pongidae to hold the great apes. Now that we know that humans and African apes are sister taxa, we should construe Hominidae differently. It is clear that the human lineage did not have a long independent evolution during the Miocene, that its origin is comparatively recent compared to other mammalian families, and that the gross genetic distinctiveness of humans is relatively low. Doesn't it therefore clarify our understanding of hominoid evolution to demote the human lineage from a family-level taxon to a lower taxonomic level?

The clade formerly known as Hominidae

The problem with this line of logic is that it is a purely aesthetic choice. There is no reason to suppose that a family-level taxon should have a particular date of origin or duration. One may argue that extant mammalian families have a distribution of ages, or even of genetic variation, and that this should inform our taxonomic choices. But the logical endpoint of this argument is not that the human lineage is a tribe-level or infrafamily-level taxon, but instead the endpoint is the conclusion of Goodman et al. (1998), that the human lineage is a subgenus-level entity and chimpanzees should be placed in Homo. The fact that this solution is viewed as "too extreme" is good evidence that this is at its core an aesthetic concern rather than a scientific one.

In fact, there is no scientific reason why a particular phylogeny should correspond to a particular range of phylogenetic ranks. Many extant families of organisms include hundreds of species, others include only one. Some extant vertebrate families originated in the Paleozoic, others in the Pliocene. And viewing only the variation of extant species is especially misleading on this issue. When we consider the relationships of extinct organisms, we find family-level groups originating across the history of the earth. The family rank has been applied to short-lived groups with uncertain affinities, to extinct collaterals of living orders or classes, and to single fossils. When it has been applied, it has usually been according to considerations of morphological adaptive pattern. On this basis, there is a good argument for the idea that the human lineage should be at the family rank, regardless of its antiquity. The adaptation to an obligate pattern of bipedalism along with the dental specializations of the australopithecines (shared with humans) set them apart from other apes to a greater extent than any great ape. These features probably mark the human lineage as substantially different from great apes in adaptive terms as the great apes are from hylobatids.

So what aesthetic considerations prevent us from simply continuing to calll the human lineage Hominidae? That usage requires that something be done to avoid a paraphyletic taxon including orangutans, chimpanzees, and gorillas. We seemingly have a choice: accept Gorillaidae, Panidae, and Pongidae alongside Hominidae, or demote all these taxa. The demotion also helps with (although does not solve, see above) the problem of assigning taxonomic ranks to the African-European ape clades. A lower-level human clade leaves more ranks below superfamily to apply to the great ape clade, its possible progenitors among the Afropithecinae or Proconsulidae, the possible ancestors of the African ape clade among the Dryopithecinae, and the possible ancestors of the human-chimpanzee clade. Each of these clades may need a rank, and there aren't enough ranks to go around.

I have no problem with aesthetic changes in nomenclature per se. After all, I wholeheartedly support replacing "Neanderthal" with "Neandertal." And in fact, I don't find "hominin" that objectionable. It may take me a while to get used to the sound of it, but it is very clear in its now-current application. Since it merely replaces the old use of "hominid," it is a simple replacement of one unambiguous term for another. It seems to me much better than relegating the human lineage to a subgenus, which would leave no taxonomic names at all to talk about the origins of the human lineage (notice how much more awkward this becomes when we can't say "hominid origins").

What I don't like is the confusion that comes from changing the meaning of "hominid." "Hominin" means nothing special to anyone now, so it has a low conceptual cost. In contrast, "hominid" until recently meant something entirely different from its proposed meaning, inclusive of all great apes. "Hominid" is how countless interested followers of paleoanthropology recognize our ancestors, and it is how many of us have presented our science publicly throughout our careers. It is bad enough that we have to get our students to understand that "hominoids" are not "humanoids," and "hominids" do not include all "hominoids." Now we have to get them to differentiate "hominins" from the rest.

An argument is that "hominin" is qualitatively more valuable than "hominid," because it conveys a more correct view of the human phylogenetic rank in comparison to other groups of mammals. This would be the "Copernican" analogy -- noting that the sun is the center of the universe "puts humans in their place," and noting that our taxonomic level is at the tribe rather than the family likewise shows how our place is less special among the species of the natural world. Or at least, it does not distort our view of ourselves by giving us a higher taxonomic rank than we deserve.

But of course, if it is our goal to have every name indicate its exact rank relative to other organisms, then we must also make mammalian groups consistent with insect groups, mollusc groups, and plants, for that matter. For this purpose, it might be as well to include a number after every taxonomic name, to represent the genetic variation encompassed by the group, or age of the group in millions of years, for example.

And more to the point, the next time someone decides that the hominoids subsume too small a segment of the mammalian phylogeny, it will seem necessary to some revolutionaries to change the taxonomy yet again. When we revise terms to give a "correct" understanding of their status, there is no end to "corrections" in pursuit of this goal.

So there are good reasons to resist the shift to "hominin." It renders "hominid" inconsistent with its historical usage in the literature. It unnecessarily confuses the public, especially those who follow our science at a distance. And most important, there is no guarantee that this change will be the last.

How does PhyloCode help?

This is not a full summary of the rules of the PhyloCode. These are available online.

PhyloCode is a system for naming clades. Under this system, each clade in the phylogenetic tree of life is eligible for a unique name. These names are not ranked, so that although clades are necessarily hierarchical, their names are not systematized in a hierarchical way. There are two basic reasons for the use of rankless names:

1. The number of clades on some phylogenies is so extensive that a rank-based classificaiton devolves into confusion.
2. Under a rank-based classification, any change in the rank of a single clade name requires concomitant changes to many other clade names, although neither their content nor their hierarchical placement has changed.

Thus, the PhyloCode "holds clades innocent" of changes in other clades, by retaining a single, unique, unchanging name for them.

Clades are may be defined in a number of ways, including by apomorphies, by descendants of a single ancestor, or by the inclusion of all species joined by a single node. This last, node-based clade definition is probably the most common. For example, the living African apes and humans belong to a clade that we might call "Clade Homo sapiens and Gorilla gorilla", while humans and australopithecines may be joined in "Clade Homo sapiens not Pan troglodytes."

Part of the appeal of this kind of scheme is that it approximates what we do much of the time anyway. The human-chimpanzee clade has no taxonomic name, at least not that most people would know, and when we talk about it, we use the term "human-chimpanzee clade." It is understood that this clade also includes Pan paniscus, and that bonobos are nevertheless not part of the name, although "human-bonobo clade" would be no less correct. For larger taxonomic groupings, this trends toward a kind of shorthand. "Human-gorilla" clade necessarily includes chimpanzees and bonobos, and it shorter than "the clade containing extant African apes and humans." PhyloCode effectively codifies this shorthand.

But at the same time it provides a procedure for giving each of these clades a name. Remembering that these clade names carry no rank information, it is possible to give every one of these clades a name that is at once unique and resistant to change with changes in our understanding of phylogeny within and outside of the hominoids.

Phylocode and hominoids

Considering all this, one may wonder what the PhyloCode proposal would say about our current taxonomic problems in paleoanthropology. In the central instance, does PhyloCode provide a way out of the hominid-hominin problem?

According to the current draft (June 2004) of the PhyloCode, "phylogenetic definitions for many widely used clade names" (Cantino and de Queiroz 2004:4) will be presented in a volume resulting from the first meeting of the International Society for Phylogenetic Nomenclature, in Paris, July 2004. That volume is not yet available, but the abstracts of the meeting have been compiled and are available in a PDF online.

Representing primate systematics at the meeting was a contribution from Kaila Folinsbee and David Begun. The part pertaining to Hominidae reads as follows:

We propose to redefine Hominidae Gray 1821 (converted clade name) as the most inclusive clade containing Homo sapiens and Pongo pygmaeus. We redefine Homininae Gray 1825 (converted clade name) as the most inclusive clade containing Homo sapiens and Gorilla gorilla not Pongo pygmaeus. Hominini Gray 1825 (converted clade name) includes Homo sapiens but not Pan troglodytes. The Ponginae has traditionally been paraphyletic, separating Pongo pygmaeus, Gorilla gorilla and Pan troglodytes to the exclusion of Homo sapiens. Ponginae Elliot 1913 (converted clade name) is defined as Pongo pygmaeus but not Homo sapiens. These converted clade names preserve the established endings of the older system in order of most to least inclusive. (Folinsbee and Begun 2004:39)

In other words, this enshrines the use of "hominin" for the human lineage and "hominid" for the great apes and humans.

I think this is unfortunate, since the opportunity was there to establish a classification that would be at the same time unambiguous and maximally consistent with historic use of the term "hominid." To do so, a different term for the great ape and human clade would have to be invented or drawn from the literature. But the strength of the PhyloCode is that this name would not have to be at a higher rank than Hominidae. So for example, all the great apes and humans could be classified in Pongidae, with the human lineage assigned to Hominidae. Retaining "hominid" for the human clade would have followed the PhyloCode recommendation for converting clade names under the old system to the new one:

Recommendation 10A. Clade names should be selected in such a way as to minimize disruption of current and/or historical usage (with regard to composition, diagnostic characters, or both) and to maximize access to the literature. Therefore, when establishing the name of a clade, a preexisting name that has been applied to that clade, or to a paraphyletic group stemming from the same ancestor, should generally be selected if such a name exists. If more than one preexisting name has been applied to the clade (including those applied to paraphyletic groups stemming from the same ancestor), the name that is most widely and consistently used for it should generally be chosen (Cantino and de Queiroz 2004:26).

Under this recommendation, the wholesale switch from "hominid" to "hominin" would not be the preferred outcome. Nevertheless, the case for resisting the classification as proposed is weak, and likely futile.

The most important consequence of the PhyloCode may be in strengthening the hand of conservatives in the future. The classification of the hominoids has for the past few decades been characterized by a pressure to place the human lineage at a lower and lower taxonomic rank. This revision began with Ernst Mayr, has continued through the elevation of "Hominidae" to include all the great apes, and is expressed today by geneticists who would like to include chimpanzees in Homo. This trend has had the primary motivation of making the hominoid taxonomy "equivalent" to that of other vertebrate taxa, with a secondary, often unstated, goal of demoting the status of humans in the natural order. There is every reason to suppose that both these motivations will continue in the future.

But the PhyloCode classification helps make it possible to retain the same names even in the As proposed, the PhyloCode recognizes the names "Hominidae," "Hominini," and others as rankless clade names. Thie means that even if the classification changes substantially in other ways (for example, placing chimpanzees in Homo), we still can use these rankless names for the clades in the hominoid phylogeny. The human lineage can be "Hominini" whether it is technically equivalent to an old-style subfamily, tribe, or subgenus, in other words. But more importantly, if rankless names are recognized widely among the mammals, then there is less of a reason to require clade names to be made consistent across the mammals. Instead, we can move to a direct reference to the age of clades, or the level of genetic differentiation they represent, or other quantitative considerations. This would be a step forward in phylogenetic classification.

Names of fossil hominid genera

Although the phylogeny of the extant hominoids is well understood, the phylogeny of fossil hominids (or hominins) is not. There are several outstanding problems, including whether the robust australopithecines are monophyletic, the relationships of the habilines, and more minor problems such as the placement of Sahelanthropus, Kenyanthropus, and Ardipithecus relative to other fossils and (arguably) extant hominoids. For these problems, PhyloCode provides some assistance.

Most important is the option to define clade names conditionally upon the acceptance of a particular phylogeny:

11.9. In order to restrict the application of a name with respect to clade composition (i.e., under alternative hypotheses of relationship), phylogenetic definitions may include qualifying clauses specifying conditions under which the name cannot be applied to any clade (see Example 1). It is also possible to restrict clade composition under alternative hypotheses of relationship through careful wording of definitions (see Examples 2 and 3) (Cantino and de Queiroz 2004:29).

This is clearly useful for the hominid phylogeny. For example, a careful definition might classify the robust australopithecines as a clade including both A. boisei and A. robustus. The node connecting these two species might well also include the species A. aethiopicus, or it might not. A definition conditioned on the inclusion of that species would encompass those phylogenetic hypotheses in which these three species are monophyletic. Such a clade might simply be named Paranthropus, or it might be desirable to give another taxonomic designation, such as "Paranthropina." The process explored by this example could easily be extended to other cases.

A question is whether this all goes too far toward the cladistic extreme of classification. There are a number of nontaxonomic names now applied to the hominids, including "australopithecine," "habiline," "human," "Neandertal," and others. Under Simpson's classification, these would be called N₂ names, and their strength is precisely that they are not taxonomic. The extension of any one of them can change according to convenience, and is not necessarily constrained by considerations such as monophyly.

There is certainly a utility to continuing to use nontaxonomic names like these, as long as adaptation is part of our consideration of evolutionary history. It is almost certainly true that humans derive ultimately from some species of australopithecine. But that does not mean that we should not talk about australopithecines, just as a definition of Dinosauria that includes birds does not mean that we should stop talking about dinosaurs.

Conclusions:

I started writing this essay while deeply considering a problem: is it time to switch to using "hominin?" This is more or less urgent to me because I have a textbook for which a decision must be made. It is not too late to search-and-replace "hominid" throughout. I have no special reason to use "hominin" myself; indeed I find it distasteful to do so. I like "hominid" -- it's the way I learned the field. And I happen to think that our adaptive differences from other primates deserve a high-rank designation, regardless of our genetic similarities.

Yet, "hominin" has a formidable position. It has swept beyond a small clique of scientists to encompass most of the new announcements of species in the field. Those most conversant in taxonomy are not the most prolific in terms of publications, but everyone who names anything must have a full understanding of these issues, and in this realm, the assault of "hominin" has been unrelenting. And within the last year popular publications have begun to regularly use "hominin." For example, National Geographic uses the term in two articles in their April 2005 issue, postfacing it as "a term for humans and their relatives."

The use of the term is no longer just an option, it is approaching the default. The PhyloCode is far from acceptance among taxonomists, but by providing a rank-free naming system for clades, it created the potential to avoid the issue. Except that the founding conference of the system introduced as an integral element the nomenclature applying "hominin" to the human clade and "hominid" to the great ape clade. So all escape routes appear to be blocked. There is only the unrelenting attrition imposed by the taxonomic cognoscenti.

All this means that if I continue to use the term "hominid," I should have a principled reason I am willing to stand by. And I don't. Nostalgia is not a principle. I myself am not confused by older literature that uses "hominid," and I am not convinced that my students will be confused, either. For undergraduates, it's just another name to learn. And if popular magazines are blithely using the term, the public is just going to have to follow. In the end, I think there will be a cost, borne by all of us, but hopefully the change will be more or less permanent and any hard feelings soon forgotten.

So sometime fairly soon, I will probably resign myself to saying "hominin," and using only my right hand on the keyboard instead of both. And maybe I'll take the edge off by writing some taxonomy myself. Any suggestions for clade names are welcome.

Afterword: Where did hominin come from?

I have never seen a review of where the usage of "hominin" came from, and how it became common in paleoanthropology. A search of journals indexed by ISI finds the first keyword reference to "hominin evolution" in a 1993 paper on Makapansgat paleoenvironment in JHE by R. J. Rayner, B. P. Moon, and J. C. Masters. The most widespread early use of the term appears to have been by Bernard Wood and his collaborators. I have not done a systematic review, if anyone has any insight on this I would be most pleased to hear of it.

References:

Cantino PD and de Queiroz K. 2004. PhyloCode: A Phylogenetic Code of Biological Nomenclature. PDF available online

Foer J. 2005. Pushing PhyloCode. Discover 26(4):47-51.

Folinsbee KE and Begun DR. 2004. Phylogenetic nomenclature of living and fossil catarrhines. In First International Phylogenetic Nomenclature Meeting Abstracts, M Laurin, ed. p. 39. PDF available online

Goodman M, Porter CA, Czelusniak J, Page SL, Schneider H, Shoshani J, Gunnell G, Groves CP. 1998. Toward a phylogenetic classification of Primates based on DNA evidence complemented by fossil evidence. Mol Phylogenet Evol. 9(3):585-598. PubMed

Rayner RJ, Moon BP, and Masters JC. 1993. The Makapansgat australopithecine environment. J Hum Evol 24(3):219-231.

In his 2003 book, Lowly Origin, Jonathan Kingdon presents a model for the origins of hominid bipedality, along with many other possible insights concerning the evolution of both earlier apes and later hominids. The book is notable because of Kingdon's speciality: as a very talented zoologist and perhaps the foremost biogeographer of African mammals, he brings an eye toward the temporal and spatial context of the transition to bipedalism that is generally lacking in other models. The book is also notable because it is recent, and provides a present-day look at many venerable models of hominid origins that well characterizes their strengths and weaknesses with respect to the present pattern of evidence.

An example of his biogeographical knowledge coming into play is his hypothesis for the place that bipedalism may have originated. Many models talk about a hypothetical division between Central African and East African forests or a hypothetical mosaic forest-savanna woodland mix. Kingdon can talk about actual forests where this might have happened. He focuses on the coastal African forest, which stretches from Somalia to South Africa (116-119). His examinations of biogeography of microfauna have shown that this forest has been biologically separate from those of Central Africa for a very long time. Today, the coastal forest is depauperate of large and medium-sized endemic mammals, which Kingdon attributes to human activity during the past 40,000 years. In the past, this forest would have served as a core area for animals spreading periodically into river valleys and forest fragments further inland. It would also have presented a rather different climate regime from the West and Central African forests, with its highly seasonal monsoonal rainfall.

Filling the bill

Any model that attempts to explain hominid origins must provide an account of several distinct things:

1. How did early hominid populations become separated from early chimpanzee populations? That is to say, what accounts for the human-chimp divergence?
2. What decisive advantage was there in increasing the frequency or importance of bipedal locomotion?
3. What exactly was the ancestral pattern of locomotion?
4. Why did this ancestral pattern, whatever it was, lose its advantages when compared to bipedality?

To question number 1, Kingdon gives basically the same biogeographical answer as Coppens' East Side Story and many others: namely, that progressive aridification of East Africa led to a separation of East and West African ancestral hominoids. His details about the nature of the East African forest are very welcome and interesting, but do not change the basic picture. Kingdon places the timing of this event in several cycles of aridity beginning at 10.5 million years ago, through recurrent drying at around 7.8 million years ago and 6.2 million years ago (119). These dates do approximately correspond with the time interval preceding the fossil remains of the earliest hominids, which are now some 6 million years old.

To the second question, about the advantage of bipedalism, Kingdon provides an answer based on Clifford Jolly's (1970) seed eaters hypothesis. In this model, and upright posture for the upper body is advantageous for use in foraging for small items, in particular seeds from grasses. Like Jolly, Kingdon envisions a squatting, ground-based ape, which he calls the ground ape. He describes the effects of a small item feeding strategy as follows:

One way of asking how apes might have responded to these limitations is to look at the feeding strategies of living species. For example, when contemporary chimps are under duress from a poor fruit season, they break up into smaller foraging units that scour the environment more thoroughly while trying to maintain their frugivorous dietary preferences for as long as possible. By contrast, the more terrestrial gorillas respond to the same pressure by maintaining their groupings but diversifying and enlarging the range of their foods to include previously ignored and less digestible plants. Another variant, better suited to eastern forests, would have been to diversify (by including more animal and underground foods) but also to spend more time and effort foraging for smaller (but still nutritionally rewarding) items. As observed in contemporary situations, these are stopgap routines for gorillas and chimpanzees. However, I am proposing that similar strategies could develop or be transposed into a sustained and systematic way of using a spatially restricted environment. (122-123)

When Jolly originated the small object feeding model, he focused on the analogy between geladas and savanna baboons as a way of understanding the effects of this dietary change. Kingdon focuses more closely on the range of plant species that may be exploited by such a dietary shift, the ability of ancient groups to exploit the same geographic range more intensively, and the probable ecological diversity of plant species in the East African forest. He notes that chimpanzee groups across Africa appear to use a similar number of fruiting plant species, adjusting their home range in response to habitat richness. This results in a great disparity in chimpanzee foraging ranges (from as little as five square kilometers to as much as 400 square kilometers). Kingdon suggests that a more intensive foraging strategy based on the wider ecological diversity of East African forests may have increased the carrying capacity of these forests for the ground apes, with consequent alterations in their social behavior and ecology. He supports this ecological model with an analysis of the species richness of human-edible plants in this eastern forest (123). His major case is based on the increased availability of ground or near-ground foods in the eastern forest, including both animal and plant resources, compared with the small ratio of time that forced chimpanzees appeared to spend foraging near the ground as opposed to foraging canopy fruits

Perhaps the most important change, in answer to question 4 above, is a change in daily foraging range. As Kingdon notes, "Quadrupedalism would never have been abandoned if substantial distances had to be covered, especially if such journeys involved exposure to predators" (125). Easy terrestrial movement and escape from predation in apes requires the rapid movement of quadrupedal locomotion. It biped faces substantial disadvantages in these respects. This means that a greater reliance on bipedal locomotion would has required both a small home range and easy access to trees. This idea is a 180 degree shift from the Darwinian model of bipedal origins, in which upright posture was a reflection of the challenges of a poor habitat and the need to forage over long distances. Here, it is safe "secure and a rich environment" that is essential to the origin of bipedalism. In Kingdon's view, living apes naturally pursue a number of hand manipulation skills, social interactions, gestural communication, and carrying objects that require them to "squat, lie down, stand on two legs, or become three-legged" (125). For all of these behaviors, bipedal locomotion might well be naturally advantageous. But chimpanzees and gorillas cannot abandon quadrupedal locomotion and its speed advantages because of their large foraging ranges and susceptibility to predation. The commitment to quadrupedalism thereby impedes the further development of manual abilities that apes already have.

This idea provides a slightly different answer from Jolly might have given concerning why geladas are not more hominid-like than they are. Although the foraging style of manipulating small hard seeds and other objects might have been similar between early hominids and geladas, the habitat is very different. Geladas must retains an effective adaptation to quadrupedalism because they do not limit their foraging to areas where trees are readily accessible. Nor do they already show the range of manipulative behaviors shared by apes, which provided further incentives to bipedalism in early hominids.

The thrust from squatting

The squat-feeding model encompasses several untested predictions, which might well provide fertile ground for research. First, this pattern of adaptation should direct attention to the anatomy of the back. In particular, to conserve energy and maximize the use of a single foraging location, the spine should be well adapted to a bright posture, flexible in side to side movements, and capable of providing a stable platform for a wide range of movement for the arms. This may help to answer the question of why early hominids had relatively long spines, and especially in contrast with very short lumbar spines in other living hominoids. It also allows the side-to-side twisting motion of the pelvis during bipedal gait to be examined as an exaptation based on an earlier ability to rotate the upper trunk against a stationary pelvis. Normal arm-swinging upright walking depends on this flexibility of the lower spine, which would appear to be absent from living chimpanzees and gorillas, in which the flat iliac blades and the lower rib cage are strongly connected and relatively inflexible. Kingdon describes the compact, inflexible trunks of living apes (127) and their disadvantages for upright walking, but he does not explore why this configuration in apes would be advantageous for the locomotor behaviors of these apes, such as climbing or knuckle-walking. This difference from hominids is worth exploring, particularly in considering the effectiveness of early hominids as climbers.

The model also places a different spin on the usual anatomical description of the changes involved in bipedalism. Generally, the shortening and broadening of the iliac blades are seen as enabling a shift in muscular action during hip extension, recruiting the gluteus maximus as an extensor of the hip instead of an abductor. Kingdon explains the shortening of the iliac blades as a way of disentangling their action from the motion of the lower trunk, creating two separate functional units. In this way, he also explains the lengthening of the lumbar spine as part of the same anatomical change. This is potentially important because the length of the lumbar spine in the common ancestor of hominids and chimpanzees is not known. If hominids descended from an ancestor with the chimpanzee-like spine, a mechanism for the expansion in length of the lumbar spine is both necessary and welcome.

One of the advantages of bipedal locomotion often cited in explanations of hominid origins is the ability to see distances over tall grass while scanning for predators. Kingdon places a different twist on this also, by suggesting that this scanning behavior was present prior to the evolution of obligate bipedalism, as the ground apes would scan for predators from a squatting position. In this way, the apes habitually made their spines as vertically erect as possible at frequent intervals, and simultaneously required effective side to side head movement. This kind of behavior may have underlain the anterior placement of the foramen magnum and the reconfiguration of the head-spine articulation. This hypothesis would especially be interesting if it were shown that the anterior placement of the foramen magnum significantly predated the origin of the pelvic specializations for bipedalism. This kind of evidence might already be present in Sahelanthropus, Orrorin, or Ardipithecus. Especially in Sahelanthropus, where Brunet and colleagues (2002) have argued for an anterior foramen magnum, and in the Aramis occiput, where the foramen magnum also appears to be relatively anterior. Pelvic evidence is not yet available from any early hominid, and although the Orrorin femora are consistent with the weight-transmission characteristics of later hominids, it is not clear that this anatomical element is necessarily reflective of an entire pelvic anatomical complex.

One might argue that every hypothesis to explain the origin of bipedalism is in some sense an umbrella hypothesis (Langdon 1997), and this is no exception. While the fundamental change hypothesized by the model is a change in foraging strategies, this change is proposed have several effects on other elements of early hominid behavior.

The first of these involves the dynamics of hominid groups. Kingdon speculates that terrestrial life would have involved new adaptations to resist a greater diversity of predators and competitors. This adaptation would likely have involved group coordination with intimidation displays. In particular, a restriction to relatively small home ranges would of reduced the possibility of simply moving on as a response to competition or predation. Climbing would have remained very important in predator avoidance, but it arguably would not be enough to cope with the eastern African ecology.

Speciation among the early hominids

Another consequence adduced by Kingdon is on the pattern of speciation of subsequent hominid lineages after the hominid-chimpanzee divergence. Kingdon describes many of the land areas bordering on the East African coastal forest, along with the prospects for ancestral hominids occupying and spreading among these different areas. He raises an interesting point about the Zambezi basin, which is largely open grassland with extensive floodplains and gallery forests and would therefore have been ideal hominid habitat despite the present lack of hominid fossils from the area.

As Kingdon describes each African region, he makes four basic points. First, the linear movement of ground apes along the coast and into the upland regions would have placed hominid populations at such distance from each other to radically restrict gene flow between them. Second, each of the areas, ranging from the Ethiopian highlands to the Zambesi basin would have presented unique ecological circumstances that would have demanded local adaptations on the part of the early ground apes. And third, the likely habitat of the ground apes extended along river courses. This means that the apes were likely not separated by the river drainages themselves, especially since many of them are highly seasonal, but instead they were separated by the interim habitats that were highly risky and resource-poor for a woodland-dependant ape. Last, the home ranges of the ground apes were probably small, again reducing the possibility of long-range dispersal and contact among populations.

I repeated the term "ground ape" repeatedly in the previous paragraph in reflection of Kingdon's other major assumption. He promotes the ground ape as a genuine stage in the evolution of the hominids. In other words, these apes once differentiated from chimpanzees were themselves highly successful occupants of the East African forest, and could themselves spread into adjacent habitats. All this occurred before the advent of of bipedalism as reflected in later hominids. This would imply that a substantial diversity of ground apes may have once existed, on the hominid lineage, but not themselves obligate bipeds. Kingdon suggests that known fossil samples like Orrorin or Ardipithecus might in fact represent a ground ape in this sense rather than bipedal hominids.

I am unconvinced by the idea that the squatting ground ape lived for a long period of time before evolving the adaptations to effective bipedality. Indeed, Kingdon's argument about the advantages of bipedalism would seem to suggest that it would emerge quickly if the opposing need for quadrupedal locomotion decreased. The idea that the ground ape stage lasted for a long time ignores the likelihood of competition from more effectively arboreal forms.

The biogeographic separation of hominid ancestors from chimpanzee ancestors (and gorilla ancestors) creates a set of interesting problems that Kingdon doesn't address. For example, if the apes on both sides of the East African arid strip were initially the same, did this original ape form survive for some time alongside the new ground apes? Or was that form itself a ground ape (as speculated below). Did this ancestral species survive alongside its bipedal descendants for some period of time? If Kingdon's idea about widespread diversification and long survival of the ground apes were true, then these apes must have coexisted for some long time with their bipedal descendants, especially if the ground apes had significant local adaptations to different African regions.

While Kingdon does support his argument that the early ground apes would have differentiated into different species with several assumptions, I found this unconvincing. Consider that chimpanzees are spread across over three thousand miles of West and Central Africa with clear evidence of recurrent gene flow among different subspecies over the past million years or more. Lowland gorillas also have an impressive geographic range, and orangutans today comprise two long-lasting geographic subspecies, which in the past must have extended to a greater diversity on the Asian mainland as well as across the Sunda shelf. The phylogenetic pattern represented by today's great apes indicates widespread species with highly conservative ecological adaptations. This allows subspecies to remain ecologically similar for long periods of time, and enables the exchange of genes long after the initial establishment of geographically distant (or periodically isolated) populations.

Kingdon does not consider this pattern, but his argument would indicate that the ground apes (or early hominids) diverged from the phylogenetic tendencies of other ape species because of their restricted home ranges and more intensive ecological exploitation of local environments. This hinges on the idea that bipedality really doesn't increase mobility, but instead radically decreases it.

But this argument fails to recognize the energetic consequences of bipedalism after it originates. It may be true that the initial transition to bipedalism would not be possible without the means of abandoning the dependence on quadrupedal movement in foraging and flight. It may also be true that obligate bipeds continued to be at a disadvantage compared to quadrupeds in predator avoidance and daily range. But the movement of bipeds over long distances would if anything have been less costly than that of a quadruped of the same size. And the social correlates of bipedality that Kingdon notes would seem likely to increase dispersal rather than decrease it. That is to say, despite a smaller home range, more cohesive groups with potentially larger group sizes present a higher chance of significant disparities in resource access among groups, a greater variance in group sizes, increased challenges for individuals integrating into new groups, and greater incentives to colonize and disperse over long distances. Bipeds are well equipped to move along linear habitats like gallery forests, and might have done so with maximum energetic efficiency in response to resource challenges or seasonal scarcity. An increased tolerance for higher population densities would have enabled an effective migration strategy in regions where seasonal resource shortfalls in one area may have been supplemented by movement to other areas with enough to go around.

This cuts to the nature of what it is to be a biped. Once the bipedal strategy arose, did it enable greater mobility or not? Were hominid groups highly territorial, and highly sedentary, or were they instead highly mobile? Did hominids tolerate local aggregations of multiple groups, or were they committed instead to intergroup conflict? This is where a chimpanzee model potentially misleads, since chimpanzees are both mobile and territorial, intolerant of contact with neighbors and capable of long-distance dispersal for maturing females. How would bipedalism change a chimpanzee's behaviors? An unanswered question.

Unanswered questions

An unanswered question is to what extent the focus on ground-accessible foods would have precluded the use of canopy foods. As Kingdon notes, canopy fruits are the major food source for chimpanzees today. Presumably, a greater adaptation to terrestrial life including bipedal locomotion would have greatly restricted the ability of early hominids to climb into the forest canopy and exploit fruiting trees. It seems possible that competition from other primates, such as cercopithecoid monkeys, might have precluded the effective dependence on a canopy resources anyway. But this line of inquiry needs to be developed further.

Another unanswered question involves the body proportions of early hominids. Australopithecines were exceptionally short compared to living humans. And there legs were hardly longer than similar-sized apes. These legs were very inefficient for bipedal movement compared to the long legs of subsequent hominids. But one possibility is that australopithecine legs may have been effectively adapted to a squatting posture. As far as I know, this hypothesis remains to be tested. Certainly if Kingdon is right about the small foraging ranges
of early hominids, the energetic disadvantages of short legs may have been relatively minor, because hominids would never have walked very far anyway. In this respect, even the home ranges of chimpanzees would be a poor model for the relatively small home ranges of early hominids. While anthropologists have tended to contrast australopithecines with early humans, who were believed to have had larger home ranges on the scale of those occupied by living hunter gatherers, it remains possible that australopithecine home ranges were smaller even than has usually been assumed.

And of course the biggest unanswered question appeared in the form of a key fossil shortly after the book must have been finished. What about Sahelanthropus? If Sahelanthropus was in fact on the hominid lineage, then it would seem to reject the model of differentiation proposed by Kingdon--Chad is a long way from the East African coastal forest. Conversely, if it is not on the hominid lineage, its importance to the model depends on what it is. If it is ancestral to hominids or to chimpanzees or gorillas, then it potentially informs us as to the anatomy of the common ancestor to these species. If so, that ancestor may have been substantially more ground ape-like than even Kingdon might have expected, at least if Brunet and colleagues (2002) are right about the foramen magnum placement and its implications for vertical posture. One might even envisage the hypothesis that chimpanzees and gorillas themselves are substantially derived from the common ancestor because they colonized the West and Central African equatorial forests long after the common ancestor lived (although presumably before the separation of chimpanzees and bonobos). This is a lot of mileage out of one fossil sample, but the absence of a fossil record for either chimpanzees or gorillas invites speculation.

References:

Brunet M, Guy F, Pilbeam D, Mackaye HT, Likius A, Ahounta D, Beauvillain A, Blondel C, Bocherens H, Boisserie JR, De Bonis L, Coppens Y, Dejax J, Denys C, Duringer P, Eisenmann V, Fanone G, Fronty P, Geraads D, Lehmann T, Lihoreau F, Louchart A, Mahamat A, Merceron G, Mouchelin G, Otero O, Campomanes PP, Ponce de Leon M, Rage JC, Sapanet M, Schuster M, Sudre J, Tassy P, Valentin X, Vignaud P, Viriot L, Zazzo A, Zollikofer C. 2002. A new hominid from the Upper Miocene of Chad, Central Africa. Nature 418:145Ð151.

Kingdon J. 2003. Lowly origin: Where, when, and why our ancestors first stood up. Princeton, NJ: Princeton University Press.

Langdon JH. 1997. Umbrella hypotheses and parsimony in human evolution: A critique of the Aquatic Ape Hypothesis. J Hum Evol 33:479Ð494.

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

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

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

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

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

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

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

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

References:

Brunet M, Guy F, Pilbeam D, Mackaye HT, Likius A, Ahounta D, Beauvillain A, Blondel C, Bocherens H, Boisserie JR, De Bonis L, Coppens Y, Dejax J, Denys C, Duringer P, Eisenmann V, Fanone G, Fronty P, Geraads D, Lehmann T, Lihoreau F, Louchart A, Mahamat A, Merceron G, Mouchelin G, Otero O, Campomanes PP, Ponce de Leon M, Rage JC, Sapanet M, Schuster M, Sudre J, Tassy P, Valentin X, Vignaud P, Viriot L, Zazzo A, Zollikofer C. 2002. A new hominid from the Upper Miocene of Chad, Central Africa. Nature 418:145-151.

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

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

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

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

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

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

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

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

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

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