gorillas

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

In the course of my research for the ape strength article, I ran across an old piece from The Atlantic Monthly, in which Alexander Young gives a long satire describing "a visit" to P. T. Barnum's "gorilla" exhibition. This article was written after the fire that destroyed the second museum.

I can't tell really whether the visit ever happened, or if the article is purely satirical. But it was an entertaining read, and looked like it might raise an interesting issue -- how much of the public reception to evolution in the United States (or even Europe, where his companies also toured) was channeled through P. T. Barnum? So I looked into it a bit further.

The part that triggered Google was this:

He was confined in an ordinary cage with iron bars of about one half inch in diameter, which seemed rather a frail barrier to those who remembered the newspaper reports which represented the gorilla on his first appearance at the Museum as bending with ease bars of five times the thickness.

In any event, the theme of the story is that Barnum's gorilla wasn't a gorilla at all.

For some time the "gorilla" rested quietly on its haunches, and seemed indisposed to move, so that I could not get a satisfactory view of him. At last he ceased to squat, and got upon all-fours, when to my mingled sorrow and delight, he switched out from under him a long tail. This was enough for me, and confirmed my previous impressions as to his character; for, though all other signs might fail, the presence of this caudal continuation proved conclusively that he was not a gorilla or any manlike ape. None of this higher class of apes are cursed with this Satanic appendage which is the mark of a greatly inferior type. A gorilla with a tail would be a monstrosity confounding all canons of anthropoidal organization, and confusing all theories of natural selection. A six-legged calf may be regarded as a harmless variation, but a tailed gorilla would be as alarming and preposterous a creation as a griffin or a centaur, and almost as unnatrual as a Yahoo or a Houyhnhnm (554).

This goes on for some four pages, by which time it has worn out its welcome. But at the end, we read a word of advice for Mr. Barnum:

I advise him to unscrew the tail of the bogus gorilla, and, if that is impossible, to cut it off, regardless of expense. Let him clutch it, as the butcher man in Holmes's poem clasped the tail of the spectre pig. Even then his sleep may be disturbed by the phantom forms and dismal groans of outraged gorillas, but he will retain the confidence of The Great American People. They may not be educated up to the belief that man is a sublimated monkey; they may not agree, with Monboddo, that the orang-outang is of the human species, or hold, with Huxley, that man is a member of the same order as the apes and lemurs, and that in substance and in structure he is one with the brutes. They may not assent to the "Development" theory of Lamarck, or the "Natural Selection" hypothesis of Darwin, and may even think that they can justly claim a higher origin than any denizen of the forest or any inmate of a menagerie. But although they may have a poor opinion of the gorilla, and hardly care to put him in their family-tree or admit him to their social circle, yet they will not submit to have him insulted by a low-lived creature who has assumed his name. They will not condemn him in his absence, and on hearsay evidence merely, but will await his arrival before they presume to pronounce upon his merits (557).

This was so curious-sounding, and gave so few details that I thought I would try to track down what the exhibit really was.

A later reference to the 1868 fire in the NY Times includes this line:

There is a legend that a naturalist who once disputed the authenticity of Mr. Barnum's ostensible gorilla, on the grounds that the gorilla was tailless, and Mr. Barnum's imitation was tailed, was crushed by being informed by the showman that the tail was sewed on. But then the spectators had never had the advantage of seeing an undisputed gorilla (Anonymous 1887).

Another reference to Barnum's museum gorilla is in the NY Times obituary for the explorer Paul du Chaillu (PDF):

In the public mind Du Chaillu has always been associated with the big monkey. As the hunter of the gorilla and entertaining introducer of that dreadful beast to civilization in the sixties, he first came into the ken of the general public. He was widely known as the man who had discovered the gorilla, because he wrote and talked so entertainingly of the big monkey, and his stories led Barnum to seek for a gorilla. To seek, with Barnum, was to speedily find. He could always find anything he wanted, animal, vegetable, or mineral. Somehow, in the gorilla matter, Barnum contrived to link Du Chaillu's name with his own.

I had thought that maybe Young was describing the famous "What Is It?" exhibit. I'll come back to that later, it's worth describing in some detail. But that would hardly have been new in 1868, having first been displayed in 1860, and in any event Young's description would have to be totally off. At one point he refers to a "dog-like face", and at another point calls the creature a "bloated baboon", so I thought maybe Barnum had in fact found a baboon and passed it off as a gorilla.

I finally found a description of the affair in the 1995 biography by A. H. Saxon, P. T. Barnum: The Legend and the Man. It turns out that Barnum himself had not acquired the animal:

Upon learning through the newspapers that the manager of his second American Museum had secured a living gorilla -- a huge baboon, he later discovered -- he immediately wrote to give expert advice on the care of this long-sought prize (Saxon 1995:95).

His advice mostly consisted of ventilation, since most of his primates had died of pneumonia. I'm sorry not to be able to get a copy of later editions of Barnum's autobiography; the first edition (on Google Books) is too early at 1855 to cover the gorilla affair. But Saxon's endnotes provide more information:

The "gorilla" in this case, as Barnum makes clear, was a patent fraud, which he invited his friend the African explorer Paul du Chaillu, then lecturing in this country, to expose and make the most of. Du Chaillu, an American and himself a controversial figure in his day, had startled the London scientific community by showing up there in 1861 with a large collection of stuffed gorillas he had shot and collected, thereby adding further fuel to the "descent of man" controversy. The bills for the second American Museum around the period Barnum writes of (1867) do indeed advertise this acquisition, touted as "the most remarkable curiosity ever presented" and the "first and only living gorilla" ever captured alive. All such advertising notwithstanding, it seems certain his museums and circuses never possessed a living gorilla during his lifetime, although Barnum repeatedly expressed his desire to obtain one. The closest he came was in 1882, when he had the offer of two preserved adult skins, which he consulted the Smithsonian about -- PTB to Spencer F. Baird, 18 September 1882, and Baird to Barnum, 28 September 1882 (Saxon 1995:359).

Well, that's enough to close the episode for me. There's a lot more interesting history there, and I'll return to it. Barnum was one of the most significant ways that people learned about zoological diversity, through exotic animals, in the late 1800's. Barnum repeatedly provoked public controversy (for profit) by promoting the idea of "missing links" between apes and man -- most famously in the "What Is It?" exhibit, which ran off and on for more than fifty years.

References:

Saxon AH. 1995. P. T. Barnum: The legend and the man. Columbia University Press, New York.

Young A. 1868. My visit to the gorilla. Atlantic Monthly 22:550-557.

Anonymous. 1887. Barnum's Bereavement. New York Times, November 22, 1887.