Miocene

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

I find myself calling her an ape.

References:

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

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

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

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

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

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

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

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

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

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

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

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

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

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

Science has a short essay by Terry Harrison this week about Miocene ape evolution: "Apes among the tangled branches of human origins."

This is the sort of article that shows just how frustrating the Miocene apes can be. It's short, probably not even 1500 words, and it has more than 20 genus names stacked into it -- and he doesn't even list Proconsul and its Early Miocene ilk.

I've been trying to give a longer account of Miocene ape evolution here, by dribs and drabs. You can get most of the list under my "Miocene" category. Last fall's account of "Late Miocene apes from Africa" expands significantly on a topic that Harrison glosses -- what do we know about African apes during the time that chimpanzees, gorillas, and humans were diverging?

There are two phylogenetic issues related to Miocene apes that command a lot of attention. Where did hominins come from? -- that's one issue. The other is, how are Asian and African apes related?

This latter question is important because it helps to establish the timeline of orangutan divergence from us and subsequent evolution. It also determines the position of the European apes -- and thereby, whether their locomotor and dietary diversity is relevant to later ape evolution.

Harrison comes down in favor of the hypothesis that Dryopithecus and most other European apes were stem hominids -- that is, collaterals of all living great apes, not specially related to the African apes and humans. The main alternative to that view is that the European apes mostly represent the African side of an early Asia-Africa biogeographic split, such that chimpanzees, gorillas and humans (the hominines) descend from Dryopithecus or some similar lineage closely aligned with these European apes. Harrison is willing to admit the Late Miocene Greek ape Ouranopithecus to the African ape lineage, but in his view the earlier European apes belong to one or more side-branches of the great apes.

A question: If Harrison is correct here, does that affect the paleontological evidence for the human-orangutan divergence? That is, if Dryopithecus were a hominine, it is plausible that the Asian/African ape divergence actually happened in Eurasia not long before 12 million years ago. If Dryopithecus branched off before the African and Asian ape divergence, and Sivapithecus was derived from an African ape, does that make the divergence earlier or later?

I'll consider that over the weekend.

References:

Harrison T. 2010. Apes among the tangled branches of human origins. Science 327:532-534. doi:10.1126/science.1184703

Time for some attention to the Miocene apes. I've neglected them for the last few years, and there have been some interesting finds. I don't mean the stuff that most people find interesting -- near-complete skeletons, or discovery of rare postcranial elements. There've been some of those, but they're European. No, I mean interesting as in African, which means potential ancestors of humans, gorillas or chimpanzees. Or all three.

This is a part of the fossil record that potentially can confirm (or disconfirm) details of the genetic comparisons between living apes. We have an increasingly detailed model for the speciation of humans and chimpanzees from their chuman ancestors. That model has been built from the complete genomes of humans, chimpanzees and macaques, and the partial genomes of the other apes. But there are potential reasons for uncertainty in the timing and duration of speciations among these living hominoids. What we need is a fossil record.

And now we have just a tiny bit of one.

Chororapithecus

I wrote about Chororapithecus two years ago on its announcement ("Did Gen Suwa just save paleoanthropology?", "More on Chororapithecus"). It's a small set of 10-million-year-old teeth from Ethiopia that look a lot like you'd expect an early gorilla to look. I don't have any new news about it, but I was reading back through the paper by Gen Suwa and colleagues (2007) and once again ran across this shocking paragraph:

Acceptance of Chororapithecus as a basal member of the gorilla clade would push back the gorilla species split to >10.5 Myr ago. Because this is a minimum date established from a meagre fossil record, the actual divergence would have predated this by an unknown time gap. From the currently available evidence, we consider that a species split of ~20 Myr ago for Pongo, 12 Myr ago for Gorilla, and 9 Myr ago for Pan are all probable estimates (see Supplementary Information). We consider that the early divergence hypothesis is congruent with both fossil and molecular data, and should be further evaluated using both sides of the evidence (Suwa et al. 2007:924).

I found that so astounding when reading it this time, that I had to go back and check what I'd written two years ago. And, blog be praised, I took good notes on it. After quoting from their online supplement (once again, grumbling that the essential details are hidden online where nobody reads them!), I concluded:

Well, that's a tricky bit of argument. We might believe that African apes never left Africa and that all the dryopithecines are therefore on the orangutan line. At least, that makes some biogeographic sense. But it's hard to argue that any of these dates are "congruent" with genetic evidence as we currently understand it. Many of the recent methods don't make any prior assumptions about "calibrated" divergence times like the orangutan-human divergence. Worse, Hobolth et al. (2007) found a human-chimp speciation time of 4 million years even considering an orangutan-human divergence of 18 million years.

The "shorter generation lengths" explanation doesn't help much -- after all, if we infer that the current great ape lineages existed as early as 20 million years ago, then almost all of the divergence time is occupied by long-generation-length species. Much faster evolution in Old World monkeys should show a strong signal of acceleration in that lineage (with a higher number of derived substitutions), and we don't see it.

If we believe these interpretations of the genes, a 10-million-year-old gorilla did not exist. Chororapithecus was something else.

Many years ago, I got used to the fact that paleontologists and geneticists live in separate realities. But this one is a real mind-bender. How somebody can blithely write that a date could be consistent with genetic estimates when the date is actually twice as old as any genetic estimate -- it's just astounding. And that we have to push all of this around for three teeth.

OK, so why am I re-reading this now? Well, Chororapithecus no longer has the only three teeth. So, it's time for a little review of the rest of the fossil record of African Late Miocene apes.

Nakalipithecus

The most substantial sample belongs to Nakalipithecus, reported by Yutaka Kunimatsu and colleagues in 2007. I didn't review that paper at the time, because it came out at the same time as our acceleration paper, so I was a little busy. The Nakalipithecus and Chororapithecus papers came out too close together for there to have been systematic comparisons of the two apes. Based on the papers -- and the brief account by Kunimatsu et al. (2007) -- the Nakalipithecus dentition is more comparable to Ouranopithecus than to gorillas.

In addition, Kunimatsu and colleagues mentioned a "large mystery ape" (my phrase, not theirs) represented by a single premolar. They wrote that this ape is more primitive and very different from Nakalipithecus or hominins. From an upper premolar, I find this idea hard to interpret -- maybe it looks like a Proconsul? They don't picture it or give measurements, so I'd say it's a genuine mystery. Maybe they are hoping to turn up more examples before they publish.

A mixed bag from Kenya and Niger

Martin Pickford and Brigitte Senut (2005) reported four ape teeth from three sites in Kenya. Three of the teeth, dating to around the same age as Orrorin, 5.9 million years ago, represent a gorilla-sized ape whose teeth look quite a bit like you'd expect an early gorilla to look, if a bit smaller.

Strangely, neither Suwa and colleagues (2007) nor Kunimatsu and colleagues (2007) mentioned these ancient gorilla-like teeth. You'd think somebody would have pointed this out. The upper molar fragment from Kapsomin looks an awful lot like the Chororapithecus holotype -- the two papers show the anatomy in profile, and the break in the Kapsomin specimen allows comparison of the enamel thickness, which is very comparable. The lower molar from Cheboit, on the other hand, doesn't look very much like the Chororapithecus lower molar, even though both are supposed to be M3. The Chororapithecus specimen looks more like a gorilla M3 -- elongated and narrower at the distal end, looking triangular in occlusal view. But the three examples of Nakalipithecus lower M3 do look like the Cheboit tooth -- all are more rectangular in occlusal shape than the triangular Chororapithecus example, two of them have a slightly lingually displaced hypoconulid. The difference is size -- the Nakalipithecus teeth are bigger, well within the gorilla range, while the Cheboit and Kapsomin teeth are at the bottom end or below that range.

Pickford and Senut (2005) also described an older molar from Ngarora, some 12.5 million years old. I think you could probably find a reasonable match for this tooth among samples of Dryopithecus -- it's the size of a chimpanzee molar but doesn't share any derived features. The authors suggest that the specimen may be an early member of the chimpanzee clade, which would require pushing the Pan-Homo divergence back before 12.5 million years ago. That's the same argument we saw above from Suwa and colleagues (2007).

Part of the reason I'm bringing this up now is a new paper by Martin Pickford and colleagues (2009), describing an ape mandible fragment from Niger. This is not the first publication on the fossil; they previously presented it in the South African Journal of Science (2008). It is a museum specimen collected in 1964 by oil geologists, and the precise locality was not recorded. The associated faunal collection allowed Pickford and colleagues to place it in the Late Miocene, but only broadly between 11 and 5 million years ago. The mandible only preserves a segment of the body around and including the roots of a first molar -- it's the right size and robustness to be a chimpanzee, but again there are no derived features, not even any occlusal anatomy on the molar. Perhaps it's Sahelanthropus' sinister twin.

I'll just mention Samburupithecus, another element of the Late Miocene African fossil ape inventory. Pickford and Ishida (1998) interpreted it as relatively derived compared to Kenyapithecus, and possibly an ancestor or outgroup to the African ape-hominin clade. At 9.5 million years old, it would predate the divergence of gorillas from the chimp-human clade, on the current molecular chronology.

Where do they fit?

OK, so after all these ape dental and mandibular remains, we come back to the question that got me started. Do any of these apes compel us to revisit the current DNA chronology?

Let's review the problem: DNA comparisons suggest that humans and chimpanzees diverged less than 5 million years ago, and gorillas a shade before that, within the last 7 million years. Against that chronology, we have three samples of fossils that are arguably hominins, from earlier than 5 million years ago (Sahelanthropus, Orrorin, and Ardipithecus kadabba), two large fossil East African apes, known from teeth, which have been compared with gorillas, and several specimens that may belong either to a gorilla-sized or chimpanzee-sized ape.

It is tempting to play "what-if" games with the chronology -- what if we changed the date of the human-chimp ancestor, for example; would the large hominoids work as members of a gorilla clade? But that's really very misleading. The genealogy of a single gene locus can be pushed around on the assumption of a different rate calibration. Models for multiple loci involving lineage sorting -- the models that we now test using genome-wide data -- involve trade-offs between speciation time, population history, rate heterogeneity, and branch lengths.

I think before I can answer the question, I will need to review two more issues:

1. What are the real constraints and confidence intervals on the genetic estimates? Just how far is it fair to push them?

2. Do we face any similar problems with the Asian apes? What about the cercopithecoids? If a single chronology works for these other lineages, the argument is less credible for a special chronological exception for the African ape-hominin (that would be hominine) clade.

So, the next post in this series will cover genetic estimates of human-chimpanzee divergence times.

References:

Bernor RL. 2007. New apes fill the gap. Proc Nat Acad Sci USA 104:19661-19662. doi:10.1073/pnas.0710109105

Kunimatsu Y and 13 others. 2007. A new Late Miocene great ape from Kenya and its implications for the origins of African great apes and humans. Proc Nat Acad Sci USA 104:19220-19225. doi:10.1073/pnas.0706190104

Suwa G, Kono RT, Katoh S, Asfaw B, Beyene Y. 2007. A new species of great ape from the late Miocene epoch in Ethiopia. Nature 448:921-924. doi:10.1038/nature06113

Pickford M, Ishida H. 1998. Interpretation of Samburupithecus, an Upper Miocene hominoid from Kenya. C R Acad Sci Paris 326:299-306.

Pickford M, Senut B. 2005. Hominoid teeth with chimpanzee- and gorilla-like features from the Miocene of Kenya: Implications for the chronology of ape-human divergence and biogeography of Miocene hominoids. Anthropol Sci 113:95-102. doi:10.1537/ase.04S014

Pickford M, Senut B, Morales J, Braga J. 2008. First hominoid from the Miocene of Niger. S Afr J Sci 104:337-339.

Pickford M, Coppens Y, Senut S, Morales J, Braga J. 2009. Late Miocene hominoid from Niger. C R Palevol 8:413-425. doi:10.1016/j.crpv.2008.11.003

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.

In last week's Nature, Russell Ciochon has a remarkable essay:

For many years, I used Longgupo to promote this pre-erectus origin for H. erectus finds in Asia. But now, in light of new evidence from across southeast Asia and after a decade of my own field research in Java, I have changed my mind. Not everyone may agree; such classifications are always open to interpretation. But I am now convinced that the Longgupo fossil and others like it do not represent a pre-erectus human, but rather one or more mystery apes indigenous to southeast Asia's Pleistocene primal forest. In contrast, H. erectus arrived in Asia about 1.6 million years ago, but steered clear of the forest in pursuit of grassland game. There was no pre-erectus species in southeast Asia after all.

I think it's interesting how much speculation Nature is willing to publish about hominid evolution in Asia. The 2005 review article by Robin Dennell and Wil Roebroeks, "An Asian perspective on early human dispersal from Africa," speculated that the origin and early evolution of Homo may have been in Asia, not Africa. And of course, several papers on the hobbits have included speculations about the pattern of early Homo in Asia, in pursuit of ways to derive Homo floresiensis from early hominids not yet found in Asia.

Ciochon's essay is part of this new tradition, but it bucks the trend. Instead of arguing that Asia was the home to an undiscovered diversity of hominids, he instead argues that the hominids have been overestimated (in part by himself) and that some fossils represent an undiscovered diversity of apes.

Ancient orangutans (Pongo) and Gigantopithecus are already known from China. Ciochon proposes a third lineage of great ape, one that would be similar to the earlier Lufengpithecus from China and Thailand:

Later, we had to field a serious proposal that Longgupo belonged to Lufengpithecus (4, 5). Although the age disparity remained troubling, the dental similarities could not be denied. I began to imagine a mystery ape as a possible solution to the problem.

The "age disparity" Ciochon refers to is that Lufengpithecus is known from the Late Miocene and very earliest Pliocene, but not the Late Pliocene. Still, if the teeth look like Lufengpithecus, it seems probable that the "mystery ape" actually is a late-surviving Lufengpithecus, or at least a close relative. Reference 5 is a paper by Dennis Etler, Tracy Crummett and Milford Wolpoff, which is available (PDF) from Etler's excellent website. Wolpoff refers to this in his 1999 book, Paleoanthropology:

The Longgupo mandible is actually a fossil ape that is related to Lufengpithecus, the missing P₃ was sectorial in shape.  However the prestigious British Journal Nature hastily published it as a hominid, with a picture of the specimen on its cover, and subsequently refused to accept papers establishing its identity.  The misidentifications actually started decades ago, when G.H.R. von Koenigswald identified an ancient australopithecine-like hominid from South China based on worn, isolated teeth, which he named “Hemianthropus.” These turned out to be worn postcanine teeth of a medium-sized Pongo species. The resemblances of the other materials to Australopithecus species were real enough, but they were not unique resemblances. A. Kramer and Zhang Yinyun have each shown there are no synapomorphies that support the hypothesis of Asian australopithecines.

So it's not a new idea that Longgupo represents an ape, or that the ape was different in size and morphology from Pongo or Gigantopithecus. It is probably natural that early paleontologists might associate these ape teeth with the hominids -- until 40 years ago, most paleontologists thought that hominids went back far into the Miocene. They were wrong, but a mistake like "Hemianthropus" was a natural one. The opposite mistake -- "Meganthropus" as an australopithecine-like hominid -- was also a natural consequence of the assumption that an unrecognized hominid diversity existed in Asia. That assumption has outlived Meganthropus, as we've seen.

Ciochon adds the idea that the ape may also be represented at other contemporary or later sites, and is apparently unwilling to attribute them to Lufengpithecus, at least not yet. He does not mention the isolated upper incisor from Longgupo, but he does appear to accept the claim that the two stone artifacts from the site are intrusive elements that are not contemporary with the jaw. The same is probably true of the incisor, which Etler and colleagues found morphologically most like living East Asians.

Ciochon suggests that some of the Hemianthropus collection may be his mystery ape:

Von Koenigswald viewed Hemanthropus as a distant relative of African Australopithecus. Later research revealed that these were worn or atypical orangutan teeth and Hemanthropus was quickly abandoned. But, had von Koenigswald actually discovered evidence of the mystery ape? In October 2005, I examined the original Hemanthropus collection. Among the many worn orangutan teeth I found several small ape teeth that very closely resembled the mystery ape teeth from Mohui. Perhaps von Koenigswald was the first to lay hands on the mystery ape.

It's not an easy task to sort through large samples of teeth trying to sort them into sets. Particularly not with these teeth -- sure, Gigantopithecus falls right out, but worn orangutan teeth aren't very easy to tell from hominids, much less "mystery apes." Ciochon ends his essay with a plan to revisit the existing samples of teeth, trying to document the variation in the mystery lineage. Sounds like a good topic for a TV show. There's a historical angle, lots of museums, a personal hook, reversal of fortune, the whole "mystery ape" thing....

Meanwhile, the introductory paragraph at the top of the post raised two issues, not one. The first is the focus of the rest of the essay: Longgupo represents a third ape in Pleistocene China; smaller than both Gigantopithecus and Pongo. The second idea is covered briefly near the end of the essay, but I think it deserves more consideration. Is it true that humans reached China 1.6 million years ago, and then "steered clear of the forest"?

Here's what Ciochon writes:

Homo erectus, it seems from this perspective, hunted grazing mammals on open grasslands, and did not or could not penetrate the dense subtropical forest. In fact, there is no record of early hominins living in tropical or subtropical forested environments in Africa or Asia.

In resolving the mystery, two other Asian sites come to mind: Jianshi (Hubei province, China) and Tham Khuyen (Lang Son province, Vietnam). At both sites, teeth labelled variously as Australopithecus, H. erectus and Meganthropus are most likely to be the mystery ape instead. Others have come to similar conclusions; a 2009 paper identifies a tooth from Sanhe Cave (Chongzuo, Guangxi province, China) as belonging to an unidentified ape.

The map accompanying the article is mysteriously depauperate of actual early hominid sites in China. Considering their locations relative to the proposed distribution of subtropical forest in Pleistocene China, I don't see an immediate objection to the hypothesis. The earliest Chinese archaeological sites, from the Nihewan basin near Beijing (Majuangou and Xiaochangliang) and also from around the Yellow River (Gongwangling and Xihoudu), are north of the Stegodon--Ailuropoda fauna. Yuanmou may have been forested at this time, but the hominid teeth there appear to be later (Hyodo et al. 2002), when the Ciochon's forest-plains biogeographic proposal may no longer hold. Josette Sarel and colleagues (2009) report on stone tools from Baerya Cave, which does preserve the Stegodon--Ailuropoda fauna, but these are so far undated and the stratigraphy has not been worked out. For all we know, the association is no clearer than at Longgupo, but that may change.

The other early Chinese sites with hominid teeth, Ciochon suggests are not hominids -- Mohui and Sanhe. Since he has examined the Mohui teeth (Wang et al. 2007), this isn't an idle speculation, and it would be odd for humans to drop their teeth around these sites without dropping a single stone tool. If he's right, that would make the earliest clear evidence of human occupation of South China into the Middle Pleistocene in age.

So, it's an interesting generalization. It remains to be seen how true it may be -- was early Homo really limited to a biogeographic strip of plains and savanna as it left Africa, or were the early humans more broadly adapted -- or adaptable?

References:

Ciochon RL. 2009. The mystery ape of Pleistocene Asia. Nature 459:910:911. doi:10.1038/459910a

Ciochon R, Long VT, Larick R, González L, Grün R, de Vos J, Yonge C, Taylor L, Yoshida H, Reagan M. 1996. Dated co-occurrence of Homo erectus and Gigantopithecus from Tham Khuyen Cave, Vietnam. Proc Nat Acad Sci 93:3016-3020.

Etler DA, Crummett TL, Wolpoff MH. 2001. Longgupo: Early Homo colonizer or Late Pliocene Lufengpithecus survivor in South China? Hum Evol 16:1-12.

Hyodo M, Nakaya H, Urabe A, Sagua H, Xue S, Yin J, Ji X. 2002. Paleomagnetic dates of hominid remains from Yuanmou, China, and other Asian sites. J Hum Evol 43:27-41. doi:10.1006/jhev.2002.0555

Sarel J, Zhang P, Weng Z. 2009. Recent discoveries in Baerya Cave (Bijie District, Northern Province of Guizhou, China). Antiquity 83 (online).

Wang W, Potts R, Yuan B, Huang W, Cheng H, Edwards RL, Ditchfield P. 2007. Sequence of mammalian fossils, including hominoid teeth, from the Bubing Basin caves, South China. J Hum Evol 52: 370-379. doi:10.1016/j.jhevol.2006.10.003

Zhu RX, Potts R, Xie F, Hoffman KA, Deng CL, Shi CD, Pan YX, Wang HQ, Shi RP, Wang YC, Shi GH, Wu NQ. (2004). New evidence of the earliest human presence at high northern latitudes in Northeast Asia. Nature 431:559-562.

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.

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!

Ann Gibbons reports on the 10-million-year-old gorilla-like Chororapithecus, elaborating on the biogeographic interpretation I mentioned yesterday:

Gorilla or not, several experts agree that an ape of this antiquity in Africa strikes a blow at a hypothesis that the common ancestor of African apes arose in Eurasia and migrated to Africa. "These are very important fossils," says Alan Walker, a paleoanthropologist at Pennsylvania State University in State College. "They show that apes have always been in Africa--that they didn't come from Europe and Asia."

Paleoanthropologists have known for decades that apes (Hominoidea) arose in Africa, where researchers have found diverse apes from 22 million to 12 million years ago. But despite many searches, almost no ape fossils have been found in Africa between 12 million and 7 million years ago, with the notable exception of a 9.5-million-year-old upper jaw from Kenya. Some researchers inferred that apes went extinct in Africa while other apes flourishing in Eurasia gave rise to the ancestors of modern African apes.

This is an important issue. I was reading a book chapter the other day that concluded that the origin of nearly every higher-level primate group may have involved rafting; in that account catarrhines originated by rafting from Eurasia to Africa, dryopithecines from Africa to Eurasia, and possibly the African ape-hominid clade by rafting or walking back to Africa. These peregrinations been a feature of hominoid evolutionary hypotheses for the last 15 years or more. Possibly it is all an illusion -- only reflecting the rarity of Late Miocene fossil apes from Africa and their abundance in Europe.

Still, the dryopithecines really do look like plausible ancestors for later apes in many ways. More on that later.

References:

Gibbons A. 2007. Fossil teeth from Ethiopia support early, African origin for apes. Science 317:1016-1017. doi:10.1126/science.317.5841.1016a

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

Chororapithecus abyssinicus teeth compared to gorilla mandible. Photo credit: Gen Suwa/University of Tokyo.

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

One of the strange things about primate evolution is the arrival of anthropoid monkeys in South America sometime during the Oligocene. South America was an island continent at the time, like Australia, filled with marsupials (even marsupial carnivores) and basal placental mammals like the sloths. And then, all of a sudden, primates showed up. It's the closest thing in biogeography to a spaceship landing and dropping off an alien race.

There is one inescapable conclusion: Thirty-five million years ago, a bunch of ancient monkeys got on a raft and sailed to South America. That's the date that comes from molecular comparisons (e.g., Schrago and Russo 2003). The earliest fossil monkeys in South America are of Late Oligocene age (Branisella boliviana), but they anatomically resemble Late Eocene monkeys from Africa (Takai et al. 2000), suggesting an earlier arrival.

A substantial debate arose over the source for these monkeys — did they arrive by raft from Africa, or from North America? Africa was farther away, but definitely had monkeys, and the South Atlantic was substantially narrower during the Late Eocene-Early Oligocene than today. North America was closer, but there is no clear evidence of anthropoids there until after the Isthmus of Panama arose 5 million years ago. So Africa seems more likely. The most likely (while still improbable) scenario is a large logjam of vegetation floating down one of the major African rivers and out to sea, with monkeys on top. They needed to survive for anywhere from a few weeks to a few months, without drinking too much sea water, to make it.

It would all seem to incredible to believe, except we know that it happened twice. Not only primates, but also caviomorph rodents got to South America during the Late Eocene or Early Oligocene (Poux et al. 2006). That includes capybaras, guinea pigs, chinchillas, and New World porcupines. Their radiation appears to have been earlier, based on earlier fossil diversification and an earlier molecular divergence date, although as yet not significantly so.

And now, a new report from Blair Hedges' lab says that frogs rafted, too (UPDATE: This link seems to be dead now, but may return; in the meantime, here's a news story). As usual, the press release precedes the actual appearance of the paper at PNAS, but it's a pretty good press release:

Nearly all of the 162 land-breeding frog species on Caribbean islands, including the coqui frogs of Puerto Rico, originated from a single frog species that rafted on a sea voyage from South America about 30-to-50-million years ago, according to DNA-sequence analyses led by a research group at Penn State, which will be published in the 12 June 2007 issue of the Proceedings of the National Academy of Sciences and posted in the journal's online early edition this week. Similarly, the scientists found that the Central American relatives of these Caribbean frogs also arose from a single species that arrived by raft from South America.

"This discovery is surprising because no previous theories of how the frogs arrived had predicted a single origin for Caribbean terrestrial frogs and because groups of close relatives rarely dominate the fauna of an entire continent or major geographic region," explained Penn State's Blair Hedges, the evolutionary biologist and professor of biology who directed the research. "Because land connections among continents have allowed land-dwelling animals to disperse freely over millions of years, the fauna of any one continent is usually a composite of many types of animals."

So rafts were heading north into the proto-Caribbean from South America at around the same time they were floating from Africa to South America.

The report talks quite a bit about how the Eocene-Oligocene date range rules out the theory that the frogs surfed on waves from the Chicxulub impact; I think that scenario seems sort of silly.

The original frogs that successfully colonized the Caribbean islands likely hitched a ride on floating mats of vegetation called flotsam, which is the method typically used by land animals to travel across salt water. "Some rafts of flotsam, if they are washed out of rivers during storms and caught in ocean currents, can be more than a mile across and could include plants that trap fresh water and insect food for frogs," Hedges said. It is not likely that the frog species dispersed simply by swimming because frogs dry easily and are not very tolerant of salt water.

The frogs are kind of a limiting case; more vulnerable to dehydration and heat than the monkeys or rodents would have been.

The thing is that these raftings need not have been rare or exceptional events; the only thing exceptional is when one happens to carry a species primed for rapid population growth and diversification. The species has to be small enough to survive for a long time on the sea with the available resources, and generalized enough to succeed on whatever resources it finds. It's the "bio" part of the biogeography that is the limiting factor -- for instance, any monkeys that crossed the Atlantic during the Miocene would have found a bunch of well-adapted platyrrhine competitors already in place. The same would be true for back-crossing to Africa. So there should be a bias toward relatively early events -- if a lineage was capable of establishing successfully by this rafting mechanism, it would have done so relatively early rather than late.

From that perspective, the interesting thing about the recurrent Late Eocene-Early Oligocene time frame is that the dispersals weren't happening much earlier. For the frogs, the answer may be habitat-related: maybe the Caribbean islands weren't great frog habitat until that time. For primates, the dispersal seems to have followed fairly soon after the appearance of anthropoids in Africa, so they dispersed to South America perhaps as early as they could have.

References:

Poux C, Chevret P, Huchon D, de Jong WW, Douzery EJP. 2006. Arrival and diversification of caviomorph rodents and platyrrhine primates in South America. Syst Biol 55:228-244. doi:10.1080/10635150500481390

Schrago CG, Russo CAM. 2003. Timing the origin of New World monkeys. Mol Biol Evol 20:1620-1625. doi:10.1093/molbev/msg172

Takai M, Anaya F, Shigehara N, Setoguchi T. 2000. New fossil materials of the earliest New World monkey, Branisella boliviana. Am J Phys Anthropol 111:263-281.

Afarensis reviews the book The First Fossil Hunters: Paleontology in Greek and Roman Times, by Adrienne Mayor:

In Chapter Three, Mayor discusses discovery of bones in the Greek Pre-classic and Classic. Classical scholars should be familiar with these in a different context. For example, the Spartan discovery of the bones of Orestes or the shoulder of Pelops kept at the sanctuary of Olympia. The bones of Theseus were discovered by the Athenians (who also swiped the bones of Oedipus from Thebes). As Mayor points out there was a veritable bone rush at that time with skeletons of heroes popping up all over the place. One of the traits that united these finds was the large size of the bones. The ancient Greeks felt that their heroes were larger in stature than they were. An idea that traces back to Hesiod's Works and Days (where he discusses the five ages of Man) and probably earlier. Over time, according to the ancient Greeks, humans have grown shorter. So when giant bones were discovered - especially those that looked vaguely human - they were interpreted as the bones of Greek heroes. The Roman emperors Augustus and Tiberius also collected bones. What unites a lot of these discoveries is that they come from areas with a lot of fossils - mainly from the Miocene to the present and composed of large megafauna such as mammoths, mastodon, giraffe and rhinoceros to name a few.

According to the review, the book includes a number of archaeological instances where fossils were found in classical or preclassical contexts. I like Afarensis' point that despite the possibility that such finds guided mythological formulations of ancient giants and the like, classical philosophers "made little mention of such discoveries."

It makes you wonder what might have been done with the same evidence and the right person. As I was reading the review, I was reminded of Thomas Jefferson and the mastodon, and I went looking up some details:

In 1784, Jefferson had bravely argued against Buffon's statement that the "mammoth" bones of North America represented the same species as those of the modern elephant. Lacking professional confidence, Jefferson successfully enlisted the support of Ezra Stiles, president of Yale College, but Buffon never wavered in his identification. Ultimately, Jefferson's position was sustained by Georges Cuvier (1769-1832), the brilliant French anatomist, who recognized the bones as those of the mastodon (Coonen and Porter 1976:747).

In the eighteenth century, those knowledgeable about fossils and anatomy to a sufficient degree to argue such facts were rare. In classical times, such people simply did not exist. Considering the spacing of natural historians in the late eighteenth century (a handful per nation-state), it is probable that no conversation could have been sustained among them without technologies, particularly printing. This is particularly true because the comparative study of such remains requires visual representations -- diagrams at a minimum; ideally casts or original specimens -- which could hardly have been distributed to a critical number of people very much earlier in time.

It's no surprise that there was some change in mindset between classical times and the Enlightenment. Still, one wonders which innovations were essential to the growth of science. As indicated by the review, classical peoples were evidently interested in ancient remains and even collected them. This acquisitiveness had increased by the eighteenth century -- with a substantial number of avocational antiquarians -- but was hardly different in character.

The interpretation that ancient mastodons and other such fossils were the remains of an ancient race of "giants" was perfectly straightforward. Although clear evidence is rare, it seems probable that every culture with exposure to such ancient bones arrived at similar mythology-inspired conclusions. In Europe and America, such explanations persisted in Jefferson's day. Even post-Renaissance antiquarians arrived at semi-mythological explanations for ancient artifacts -- for instance, ancient stone tools as "thunderstones." Most straddled the boundary between mythology and naturalism.

The Enlightenment was the first point at which the tide of science was capable of formulating and testing a coherent alternative. The fossil record provided clear evidence directly on the origins of the earth and its history, and the logical options were clear enough once some connection between rock layers and time was made. As an example, Jefferson already knew enough to predict overkill as a cause for the disappearance of ancient megafauna:

Jefferson argued that an animal as large as the "great-claw" [the giant sloth] must always have been rare because, he reasoned, the "ordinary economy of nature" would provide "sufficient barriers" to large populations:

If lions and tygers multiplied as rabbits do, or eagles as pigeons, all other animal nature would have been long ago destroyed, and themselves would have ultimately extinguished after eating out their pasture (Jefferson 1799, p. 256)

Referring to Africa, Jefferson also claimed that a "new population" -- namely, man -- tended to drive off large animals to the continental interior. He suggested that in North America the pressure of Indian hunters had accomplished the same shift. This analogy was the rationale behind his seemingly whimsical instruction that Lewis and Clark look for signs of the living mammoth west of the Mississippi. Furthermore, Jefferson hinted that, by preferential hunting of these giant animals for an obviously great store of meat and hides, the Indians had probably exterminated them (Coonen and Porter 1976:747).

Two assumptions had crystallized by the eighteenth century: exponential (or "Malthusian") growth of populations, and the progressive decay of ancient things. Both assumptions are products of everyday observations that may have gotten more ordinary over time.

Old cities decay and are replaced; old things are buried and unburied. Sometimes the cities themselves get higher as a result -- a fact increasingly known as excavations into the subterranean layers of cities (for foundations and sewers) increased. The classics surely knew these things, but the recognition of old things must have grown as human history piled itself up into deeper and deeper layers.

The fleeting nature of life and youth was a standard of classical authors, but the disappearance and decay of entire civilizations was particularly part of the Enlightenment zeitgeist. Perhaps it was no accident that the beginnings of paleontology coincided with Edward Gibbon's Decline and Fall of the Roman Empire. Lost signs of ancient things became a staple of early Romanticism, and several scenes in Wordsworth's work wear on the implications of hidden histories. Better-known is Shelley's "Ozymandias," written in 1817:

I met a traveller from an antique land
Who said:—Two vast and trunkless legs of stone
Stand in the desert. Near them on the sand,
Half sunk, a shatter'd visage lies, whose frown
And wrinkled lip and sneer of cold command
Tell that its sculptor well those passions read
Which yet survive, stamp'd on these lifeless things,
The hand that mock'd them and the heart that fed.
And on the pedestal these words appear:
"My name is Ozymandias, king of kings:
Look on my works, ye mighty, and despair!"
Nothing beside remains: round the decay
Of that colossal wreck, boundless and bare,
The lone and level sands stretch far away.

A paleontologist reading the poem may find that it evokes a great fossil eroding from a desert badlands; replace "Ozymandias" with "Tyrannosaurus", and the verse sums up the present-day attitude toward the dinosaurs, far more than that toward ancient Egypt.

Imperial Rome, at over a million souls, was the apotheosis of classical population growth, but a clear reflection on the implications of such growth may have needed post-medieval mathematical insights or monetary and economic insights. London reached its first million shortly before 1800 -- the first city to do so since classical Rome. By that time, economics and mathematics were ready to infer the consequences of rapid population growth.

We now know that both insights were necessary for evolutionary theory to emerge, and the strands of evolutionary thought emerged before Darwin in the Enlightenment. This short-term history of thinking in the eighteenth and nineteenth century certainly benefits from considering just how much had changed in human existence since classical Greece and Rome.

References:

Coonen LP, Porter CM. 1976. Thomas Jefferson and American biology. BioScience 26:745-750.

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.

One of the most important mechanisms of genetic evolution is gene duplication. There are a few well-known gene families, such as the globin gene family, whose several members have diverged over hundreds of millions of years from a single ancestral gene. Each globin gene is the product of one or more duplications.

Googling through some papers, this line got my attention:

The divergence of gene expression between human duplicate genes is rapid, probably faster than that between yeast duplicates in terms of generations.

That's from Makova and Li (2003). You have to admit, it's attention-getting. Human gene expression differentiating faster than yeast?

It's about genes that have duplicated during recent evolution. When one gene becomes two, the tendency is to think the newly arrived copy will be neutral. But things are not simple -- two copies of a gene complete with associated regulatory sequences may end up making twice as much of the gene product. Occasionally that may be a good thing, but often it will be bad. So selection affects gene duplicates the same way it affects anything else.

But duplicate copies of genes present an interesting possibility: they may come to be regulated differently. This can happen if both copies retain their regulatory machinery, but some part of the regulatory chain of one copy is changed by mutation. Or it can happen if the gene duplication does not duplicate all the regulatory sequence -- for example, if it is located some considerable distance upstream from the original copy.

Makova and Li (2003) examined one kind of change in gene expression -- when different copies start to be expressed in different tissues. This kind of change is fairly easy to understand in terms of regulatory sensitivity. Different tissues express different regulatory proteins and RNAs, and regulatory sequences of genes are more or less sensitive to these different parts of the regulatory machinery. Sequence rearrangements may displace the coding sequence farther from inhibitor sites, or may decrease the chance of methylation, or may place the new copy next to a highly transcribed region. Sequence changes can remove an enhancer site, or make a transcript more susceptible to RNA interference, or any number of other changes. There are many, many possibilities for regulatory divergence.

The timescale of expression divergence studied by Makova and Li (2003) is fairly long:

We found that a large proportion of human duplicate genes have diverged rapidly in their spatial expression. Assuming that the average synonymous rate in higher primates is 1.5 x 10^-9 nucleotide substitutions per site per year (Yi et al. 2002), 75.5% of human paralogs diverge in their expression in at least one tissue after only 25 Myr (K_S = 0.068).

Clearly, "rapid" is a relative term. Here, we are looking at functional divergence of duplicate genes over the time occupied by the divergence of the hominoids from early Miocene apes to the present. Some proportion of these changes have occurred during the past few million years of human evolution, and may be among the genetic changes that led to the evolution of human-specific characters.

However, the broadest functional category represented by genes that differentiated functions after duplication was immune response:

It is interesting to look into the functions of duplicate genes that show rapid divergence in expression. Thus, we investigated the functions of the duplicate gene pairs with KS < 0.3 and with diverged expression (as presence or absence of expression in a tissue) in at least 50% of the tissues studied (we considered only the tissues in which at least one gene of a pair is expressed). There were 38 such gene pairs (Table 1). Also, we examined duplicate gene pairs with KS < 0.3 and a correlation coefficient of gene expression (R) < 0.5. There were 18 gene pairs in this group (Table 1). Interestingly, most of the gene pairs in these two groups overlapped. Thus, the results from the two measures concur. The functions of these genes were retrieved from LocusLink (http://www.ncbi.nlm.nih.gov/LocusLink/) manually. The gene pairs in these two groups encode enzymes (oxidoreductases, hydrolases, transferases, and an isomerase), proteins of the immune system (e.g., lymphocyte antigen, cytokine gro-beta, MHC proteins, and immunoglobulins), transcription factors, structural proteins (e.g., amelogenin, keratin, and skeletal muscle protein), and receptors (Table 1). To determine whether any of the functions were overrepresented among genes with rapid divergence in expression, we compared their functions with the functions of the other duplicate genes using the Gene Ontology database (Camon et al. 2003). There was indeed a significantly higher proportion of immune response genes among gene pairs with rapid divergence in expression compared with other gene pairs in our study (P < 0.009 for gene pairs with KS < 0.5 and diverged expression in at least 50% of studied tissues; P < 0.001 for gene pairs with KS < 0.5 and R < 0.5).

They also found that two-thirds of the duplicate genes that didn't diverge in expression were genes that are normally expressed in nearly all tissues -- in other words "ubiquitously expressed" genes. This finding has been confirmed by later work (for example, Yang, Su and Li 2005; Liao and Zhang 2006). Liao and Zhang (2006) showed that the degree of evolution in gene expression profile is negatively associated with gene expression level -- that is, more highly expressed genes evolve more slowly. This is paralleled by the observation that sequence evolution is slower for more highly expressed genes. Yang et al. (2005) showed that narrowly expressed genes (those expressed in few tissues) evolve faster than those expressed more broadly.

All these observations tend to support the idea that pleiotropic constraints are important limits to adaptive evolution. Gene duplication followed by functional divergence is one of the main ways that genetic correlations among different phenotypic characters can be decoupled. If a gene duplication can allow a single gene with two phenotypic effects to become two genes each with one phenotypic effect, then it can erase pleiotropic constraints on evolutionary change.

It's a way of opening new pathways to the evolution of complex phenotypes.

About the yeast thing: Naturally, the possibilities for regulatory divergence are higher in vertebrates than in yeast. Vertebrates have substantial differentiation of tissue types, complex developmental programs, and differential gene expression. So it's no real surprise that vertebrates should have seen more rapid regulatory evolution than yeast in this respect. But it does show that this kind of duplication and subsequent functional differentiation is a potentially rapid pattern of evolutionary change compared to other patterns of change.

References:

Liao B-Y, Zhang J. 2006. Low rates of expression profile divergence in highly expressed genes and tissue-specific genes during mammalian evolution. Mol Biol Evol 23:1119-1128. doi:10.1093/molbev/msj119

Makova KD, Li W-H. 2003. Divergence in the spatial pattern of gene expression between human duplicate genes. Genome Res 13:1638-1645. doi:10.1101/gr.1133803

Yang J, Su AI, Li W-H. 2005. Gene expression evolves faster in narrowly than in broadly expressed mammalian genes. Mol Biol Evol 22:2113-2118. doi:10.1093/molbev/msi206

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!

Well, it hit Slashdot, so here goes:

Snakes as agents of evolutionary change in primate brains

Lynne A. Isbell

The abstract is really long. I'm going to quote all of it, but I'm separating into sections and adding numbers [in brackets] for further comment:

[1] Current hypotheses that use visually guided reaching and grasping to explain orbital convergence, visual specialization, and brain expansion in primates are open to question now that neurological evidence reveals no correlation between orbital convergence and the visual pathway in the brain that is associated with reaching and grasping. An alternative hypothesis proposed here posits that snakes were ultimately responsible for these defining primate characteristics.

In other words, you can reach and grasp with one eye closed. More below.

[2] Snakes have a long, shared evolutionary existence with crown-group placental mammals and were likely to have been their first predators.

Opportunity.

[3] Mammals are conservative in the structures of the brain that are involved in vigilance, fear, and learning and memory associated with fearful stimuli, e.g., predators. Some of these areas have expanded in primates and are more strongly connected to visual systems. However, primates vary in the extent of brain expansion. This variation is coincident with variation in evolutionary co-existence with the more recently evolved venomous snakes. Malagasy prosimians have never co-existed with venomous snakes, New World monkeys (platyrrhines) have had interrupted co-existence with venomous snakes, and Old World monkeys and apes (catarrhines) have had continuous co-existence with venomous snakes.

Not obvious that brain expansion and conservative fear pathways are really related to each other. Since there are many interconnections between different brain regions, it is not at all persuasive that some of the brain areas connected to fear response and learning are connected to neocortical areas that evolved within primates.

[4] The koniocellular visual pathway, arising from the retina and connecting to the lateral geniculate nucleus, the superior colliculus, and the pulvinar, has expanded along with the parvocellular pathway, a visual pathway that is involved with color and object recognition. I suggest that expansion of these pathways co-occurred, with the koniocellular pathway being crucially involved (among other tasks) in pre-attentional visual detection of fearful stimuli, including snakes, and the parvocellular pathway being involved (among other tasks) in protecting the brain from increasingly greater metabolic demands to evolve the neural capacity to detect such stimuli quickly.

Interesting...although the connection to snakes ("fearful stimuli, including snakes") isn't exclusive.

[5] A diet that included fruits or nectar (though not to the exclusion of arthropods), which provided sugars as a neuroprotectant, may have been a required preadaptation for the expansion of such metabolically active brains.

Possibly true, no obvious snake influence.

[6] Taxonomic differences in evolutionary exposure to venomous snakes are associated with similar taxonomic differences in rates of evolution in cytochrome oxidase genes and in the metabolic activity of cytochrome oxidase proteins in at least some visual areas in the brains of primates.

Interesting. But the number of primate lineages compared is only three (anthropoids before platyrrhine/catarrhine divergence, and platyrrhines vs. catarrhines after divergence). And the same relation could be explained in terms of brain size alone (if larger brained lineages need greater COX activity).

[7] Raptors that specialize in eating snakes have larger eyes and greater binocularity than more generalized raptors, and provide non-mammalian models for snakes as a selective pressure on primate visual systems.

I wonder why this is -- does it have to do with the motion patterns of snakes compared to other raptor prey (like quick-moving small mammals)? Or the shape and coloration of snakes against likely backgrounds?

[8] These models, along with evidence from paleobiogeography, neuroscience, ecology, behavior, and immunology, suggest that the evolutionary arms race begun by constrictors early in mammalian evolution continued with venomous snakes. Whereas other mammals responded by evolving physiological resistance to snake venoms, anthropoids responded by enhancing their ability to detect snakes visually before the strike.

Unanswered questions

I have to say, I approached this one very skeptically, but after reading it I have a lot of sympathy for the approach. But to start off, I will be very clear about questions that someone might reasonably ask that the paper really doesn't have great answers for:

The paper devotes a section to this question. There have been some observed or suspected instances of snakebite in wild primates, and humans suffer a lot of snakebite -- especially in the tropics. But there just aren't any good numbers, such as relative importance of snakes compared to other predators or mortality risks.

My own feeling about this is that snakes probably are a significant risk to wild primates, but that they are one of many such risks. So the question is whether selection favored effective responses to snakes in particular or instead responses to many predation risks in general.

Distinguishing general from particular is a pretty hard problem -- most of the visual pathways discussed in this paper are useful for detecting all kinds of things, not merely snakes. For example, the paper includes this:

With its emphasis on object recognition, the P pathway would have initially helped those with a diet of fruits, flowers, and nectar to locate foods (and perceive snakes and other salient objects near them). Later, with its emphasis on color, the P pathway would have helped such primates locate foods with the highest levels of sugars (Sumner and Mollon, 1996), thereby more effectively protecting the expanding brain against excitotoxicity.

Or, maybe finding fruits just happened to help evade likely predators including snakes. In other words, there may be a link, but the direction of causation is far from clear.

All overarching single-cause hypotheses face this problem: the things they want to explain almost always happened at different times. Here, we have the evolution of larger brains and arboreality early in the Cenozoic (or even the Cretaceous), the evolution of the visual system through the Eocene and Oligocene, the evolution of brain size in different catarrhine lineages during the Oligocene and Miocene, and so on. This paper plays that problem as a strength: snakes plausibly exerted a mortality pressure across all those time intervals, when other hypotheses like nocturnal insect hunting didn't apply to most of them. On the other hand, nocturnal insect hunting doesn't really try to explain later events. A single grandiose over-arching hypothesis may claim a strength that it explains more things, but that is no substitute for testing each of its components. The relationships proposed here are plausible, but few of them admit any ready tests.

So those are some problems for the hypothesis that the paper really doesn't answer well. It might well be that snakes really were such an important mortality risk that ancient primates had adaptations specially to defend against them, and that those adaptations themselves contributed to later primate evolution. But it's not easy to sort out the causes -- maybe those apparent "snake-adaptations" were really initiated for other purposes and happen to be useful for resisting snakes, or maybe they really don't have much to do with snakes one way or the other.

Stuff I liked

But there's lots of clever stuff in this paper, making surprising connections between visual processing, diet, and predation risk. For example, I like this:

The hypothesis that constricting snakes favored larger brain size via greater visual specialization in primates identifies a diet of ripe fruit or nectar as a requirement for, and as a cause of, visual specialization and brain enlargement, but not as the ultimate cause. Recall that high CO [cytochrome oxidase] activity reflects high levels of neuronal metabolic activity and that brains are highly metabolically active tissues. Heightened CO activity is, however, potentially costly in that it can lead to excitotoxicity and neuronal death (Lucas and Newhouse, 1957, Olney, 1969, Olney, 1990, Choi, 1988 and Meldrum and Garthwaite, 1990) without protection against overexposure to glutamate, the main excitatory neurotransmitter in the central nervous system (Orrego and Villanueva, 1993). Glutamate is an amino-acid derivative of glucose (Feldman et al., 1997: 392), and it has widespread effects on the brain. Of particular relevance here is its ability to enhance fear-related learning in the amygdala (Walker and Davis, 2002) and to enhance learning in color discrimination tasks (Popke et al., 2001).

Overexposure to glutamate can be minimized by eating glucose, a sugar found in flowers and ripe fruit (Henneberry, 1989, Romano et al., 1993 and Guyot et al., 2000). If frugivores indeed have larger brains and higher basal metabolic rates than folivores or insectivores of the same body size (Clutton-Brock and Harvey, 1980, Armstrong, 1983, Barton et al., 1995 and Martin, 1996), the difference could be a result of the neuroprotectant property of glucose, obtained from a diet of fruits and flowers.

It seems like fruit-seeking behavior would be adaptive for a primate that maintained high cytochrome oxidase levels, not only globally but in local brain regions (here, the visual system is the focus, but possibly other regions might be implicated). People tend to take for granted that sugar-rich foods would be good for primates, but that is really not obvious -- fruits tend to have low protein levels, for example. So an evolutionary specialization on fruits has costs, and it is important to sort out how and why early primates bore those costs.

The paper has a really good section (called "Frequently asked questions!") that presents strong critiques of a couple of oft-cherished theories of primate evolution. It argues that the "nocturnal visual predation" hypothesis is weak because there is evidence that the key primate characteristics ("orbital convergence, enhanced vision, grasping hands and feet, nails, and large brains") did not evolve together.

And I love this paragraph in the "What about sociality" section:

First, [the social intelligence hypothesis] must explain why sheep (Ovis aries), which are not known for having large brains, are still able to visually recognize and remember as many individuals as there are in a typical baboon group, even after a year of separation (Kendrick and Baldwin, 1987 and Kendrick et al., 2001). In both primates and sheep, the temporal cortex is a major site of facial recognition and memory (Gross et al., 1972, Damasio et al., 1982, Perrett et al., 1992, Kanwisher et al., 1997 and Kendrick et al., 2001).

This is a telling sentence:

Critics of the inclusiveness of this [snake] hypothesis are challenged to explain why it would be easier, or more likely, for primates to evolve large bodies or large, complex groups in response to predators than to modify the mammalian visual system in response to the same threat.

There has been a lot more attention to the evolution of brain size, body size, and group size, and comparatively little to the evolution of the visual system (aside from color). Primates have long life spans compared to other mammals, which means that primates have low average mortality rates as adults. One way to get low mortality is to maximize avoidance of predators. To the extent that large brains facilitate evading predators, they will be correlated with low adult mortality. To the extent that large social groups resist predation, they will be correlated with larger brains.

The interesting relations must be inside the brain -- for instance, are larger neocortex sizes specifically adaptations to group living? Or are they involved with interpreting and acting upon visual signs? Visual signs would include those associated with predators, foods, and other individuals. It's not obvious to me that visual cortex allometry is going to give you a good test of these relations, since adaptation would require interpretation and action upon visual signals, and not merely sensing them.

Anyway, those are some thoughts on the primates vs. snakes paper.

References:

Isbell L. 2006. Snakes as agents of evolutionary change in primate brains. J Hum Evol 51:1-35. DOI link