Miocene

Bernard Wood and Terry Harrison have published a review paper in Nature[1], arguing that the extent of anatomical convergence among Miocene apes makes it difficult to reconstruct their relationships. The keyword of their essay is "homoplasy", a word for the situation when characters evolve convergently, in parallel, or in reverse. When parallelism or convergence have been common enough, we will find it difficult to use morphological characters to test hypotheses about the phylogeny of species. The butt of their essay is Ardipithecus, with extension to Sahelanthropus and Orrorin:

We emphasize that we are not claiming that the presence of homoplasy in and around the hominin clade, and the other methodological and analytical limitations of phylogenetic analyses noted above, doom all efforts to recover evolutionary relationships to failure. Nor are we claim- ing that Ar. ramidus, S. tchadensis and O. tugenensis are definitely not hominins. We do, however, advocate that those palaeoanthropologists whose considerable and much valued efforts in the field are rewarded with fossils as significant as those from Aramis, Toros Menalla, Lukeino and Malapa acknowledge the potential shortcomings of their data when it comes to generating hypotheses about relationships.

The main points won't be news to many readers. One long-time correspondent called the essay "idea homoplasy", focusing as it does on the same issues that I covered here in 2009, and the evidence for craniodental parallelism among Miocene apes that we reviewed in our 2006 paper on Sahelanthropus [2]. That's probably too kind respecting my role in this matter, but I suppose it is one of the chief drawbacks of blogging that I pass by many of these opportunities to do perspective and review articles for top-tier journals. But still, why wait two years to make a point that can really be made in an afternoon, and reach many, many more readers? I mean, Nature wants $32 for this review. Seriously.

I find it nonetheless interesting to see Nature take up the subject, however belatedly, and Wood and Harrison ably cover some of the problems of convergence in Miocene apes. Harrison is an expert on Oreopithecus, and the paper includes four paragraphs describing its relevance to the topic of homoplasy in fossil apes. To me, this is a key comparison that deserves a longer treatment. You can find a bit more information in my 2009 Ardipithecus coverage ("The Ardipithecus pelvis"), but I'm not really the person to do a thorough job of it. I would hope that someone will return to the issue at greater length, but I think that would require access to the Ardipithecus pelvis reconstruction, which is not available for independent inspection.

In light of the Pliocene goat-man lunacy the other day, Daniel Lende ties the satire directly to this little Ardipithecus dustup. He points to the dueling quotes in this Science News article by Bruce Bower:

“Researchers have to stop publishing papers that say, essentially, ‘This fossil is an early hominid, so suck it up and accept it,’” [Bernard] Wood says. “Nature and Science could change this practice overnight if they wanted to.”

...

“With no new data, no new ideas, no new methods, no new hypothesis, no new experiments, no new fossils, not even a new classification, this paper will leave everybody wondering what’s happened to the peer review process at Nature,” [Tim] White says.

And then there's the write-up by Katherine Harmon, who pulls quotes from Nature's podcast on the paper:

Tim White, of the University of California, Berkeley, and one of the lead authors on the 2009 Ardi papers, called the new article a "six page illustrated op-ed piece" in the Nature podcast. He maintains that "whole functional complexes"—not just individual characteristics—that were described in his team's papers link Ardi to humans "to the exclusion of the great apes."

Oh, goodness. I'm not entirely sure what is to be done about these folks. The thing about the 17-year inquiry into the "one large goat" theory, is that I bet they made the CT reconstructions and dental measurements of the goat-men available for inspection.

References

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

I find myself calling her an ape.

References:

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

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

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

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

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

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

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

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

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

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

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

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

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

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