Friday, March 30, 2012

Forget bipedalism. What about babyism?

First, a little time travel experiment...

Here's a newspaper headline and blurb from 709,987 CE: 

Hominin fossils dated to 2,012 CE show arboreality

Artists have made a realistic reconstruction (above) of an early human species based on the anatomy of the latest fossil discovery in paleo-Alabama by a team of paleontologists. These primitive hominins were still climbing trees!

In yet another reconstruction of this primitive species (above), an adult forages for honey by scrambling nimbly up a tall tree trunk. 

In other paleontology news, a team of scientists determined that a Morrocan variety of domestic goat, from roughly the same primitive era, could adeptly climb small bush-like trees.

I promise that's not sarcasm or postmodernism! That's just me trying to jossle you loose of some traditional assumptions and spark you to wonder about how we know what we know about the functional relationships between anatomy and behavior.

I'm thinking about this because of the latest and greatest news in the world of paleoanthropology, published this week in Nature and here's a nice video to bring you up to speed:

If this Burtele foot fossil represents a hominin, it's different enough in anatomy (and the functional interpretation of that anatomy) to be considered something separate from other hominins on record.

It's this whole other animal.

As of now, all hominins at this time in the mid Pliocene (the foot is dated to 3.4 mya) belong to the genus Australopithecus and are only known from sites in East and South Africa. Perhaps the Burtele foot is another species that is not A. afarensis (which supports long-existing arguments that there are two lineages at this time) or maybe this is an ancestor to the Paranthropus radiation that occurs in the early Pleistocene. Or maybe it's not even a hominin, because the foot is very ape-like. Moreso than any australopiths on record.

Chimpanzee displaying it's non-human-like hallux (big toe). 
Can we tell what this animal is? Without teeth and cranial bones--our gold standard for identification and distinction--can we surmise what kind of creature this Burtele foot belonged to?

For starters, if it's to be deemed a "hominin," we should determine what exactly about this foot is human-like.

In terms of metrics, the Burtele foot shares traits with humans but these are also shared by gorillas and sometimes chimpanzees and sometimes old world monkeys too. The striking similarities between human and gorilla feet have been known since the earliest comparative anatomy studies and it was only a matter of time before a new primitive fossil brought the problem to heightened prominence.

For the qualitative traits, more similarities appear to be shared with the famous "Ardi" skeleton from about a million years earlier in time (belonging to Ardipithecus ramidus) than with extant humans.

According to the paper, there appears to be few derived, hominin-specific features in this foot. And that's even if you are on board with calling Ardi a hominin. Granted, we expect more primitive hominins to share few of those traits with us and traits evolve mosaically, even within the foot. And granted, not all hominins contributed directly to our evolution, so we might find species on the hominin branches of the TOL that share no derived features with humans. Still, the case isn't very strong for this Burtele foot being a hominin.

One of the reported hominin-like traits has to do with the shape and orientation of the proximal phalangeal joint where it articulates with the second metatarsal head. This appears to indicate that the foot was experiencing more toe-off during walking, more like human walking than like ape walking since it's not the condition found in ape feet. This functional interpretation seems to be based on that made of Ardi's foot. Unfortuantely I don't think anyone's looked at the biomechanics of this joint in apes (and ape feet) as they walk bipedally, yet. (But I could be wrong!)

Also, although the degrees of torsion in the second metatarsal is ape-like, the torsion in the first metatarsal is more humanlike. (Torsion describes the orientation of the proximal joint surface relative to the orientation of the head. The Burtele foot's MT2 and MT4 are reported to have less torsion than that seen in African apes (where this is associated with a grasping orientation), yet are still significantly twisted compared to human metatarsals.)  The torsion in the big toe (hallucial metatarsal) is reported to be unlike that of African apes, and presumably more like humans? It's not clear. But the actual measure of the degree is not included in Table 1, nor is it demonstrated in the Supplemental section as implied. So we have to take their word for it. And by the look of the Burtele first metatarsal in the photos, that's probably not a problem.*

So there are some leads away from extant African apes and weak ones toward Ardipithecus and possibly extant humans, but what the paper demonstrates better than the hominin status of the Burtele foot is just how difficult it is to pin down hominin-ness.  We don't always know it when we see it.

For most of us and I assume the authors of the paper, this is what makes paleoanthropology so fun! But it's also why we fight.

That's not because we don't know how anatomy and behavior are linked in extant humans, apes, monkeys, etc... we seem to have a pretty good handle on that. At least big picture. The problems arise when you zoom in. Are chimpanzees really arboreal? Yes. Are they really terrestrial? YES. Same for gorillas.

So reconstructing an evolutionary scenario in which our hominin ancestors went from a state of arboreality to a state of terrestriality is not that simple. The Burtele foot describers definitely understand this. It's just the popular media that doesn't have the time or the inclination to get this. Hence my intro above.

But that intro up there with the futuristic newspaper wasn't purely reaction-against-media-reaction. It's also me reflecting on issues closer to home for paleoanthropologists.

Do primitive "arboreal" traits in hominin skeletons really correlate with arboreal behaviors? Or are they ancestral relics? We don't do much climbing anymore but we have all kinds of anatomy that links us to our tree-hugging relatives, and presumably to our shared tree-hugging ancestors.

So at what point do we recognize primitive traits as being only that? Why must all traits we observe in extinct animals be so USEFUL?

The answer is.... because that is the only way to go about these functional studies. By definition functional anatomy indicates FUNCTION. So we go in with a bias toward identifying function, NOT with an aim to identify primitive relic anatomy that just happens to work for the animal. The latter is so much harder to perceive although one might argue it's what our null hypothesis should be. It's easier to assume that if an animal has the anatomy, then it's functional and therefore it's "for" doing whatever it is that it does with that anatomy.

Who cares about these subtly different approaches to comparative anatomy and evolutionary reconstruction?

Well if you're trying to determine when bipedalism became habitual and when hominins stopped relying on trees for foraging, fleeing, socializing, and nesting, then it matters whether functional anatomy is function or whether functional anatomy is just hanging on. (pun intended) Welcome to the nightmare that is paleoanthropology!

So where does the Burtele foot leave us?
1. Looks like we've got a separate ape-y thing that's not Lucy's species (A. afarensis) living around the same time and place as Lucy and her ilk.
2. Looks like whatever this animal is it doesn't have the few derived features found in some australopith feet. (those are even debated...)

But speciation, co-habitation, and bushy hominin phylogenies aren't even the coolest part of this story.

The two distinct foot morphs offer another kind of insight.

Lemme show you.

First of all, what is arboreality and how much arboreality is enough to require specific grasping adaptations in the big toe?

We know that cercopithecines (like macaques and baboons) vary pretty widely in their degrees of arboreality and terrestriality, but regardless, they're good in the trees and they're good in the trees despite their short and diminutive big toes! Arboreal behavior can be accomplished via many different evolutionary processes revealed to us via skeletal anatomy.

Here are two baboons showing off their small big toes.

Baboons are considered to have terrestrial adaptations in their feet that are similar to those in humans like with their shorter phalanges, but they're also the opposite of humans with their short, not long big toe.  Like with arboreality, terrestriality works via many different evolutionary processes that are revealed via the skeletal anatomy...and this goes beyond primates. (The crux of it all for human evolutionary reconstructions is determining how bipedal terrestriality differs from quadrupedal terrestriality.)

Gibbons (apes) are super aboreal, but their locomotion biases grasping hands, not feet. However, their suspensory behavior does use the grasping big toes.

Here are some gibbon feet displaying their big big toes.

Here's a film showing a gibbon using its grasping big toe:

Conclusion: The arboreal use of the strong grasping big toe is not necessarily about climbing or even walking on tree limbs;** it's probably more about suspension.  Suspensory behavior is typified by the gibbons, orangutans (many at least), and the rest of the apes and so is the grasping big toe. That's the strongest functional explanation for the ape's thumblike big toe.

Now, larger apes are not suspending as much with their toes. And they can get up into the trees just fine without grasping with their big toe.****

DeSilva (2008)
So think about who's doing much of the suspension particularly in African apes: Juveniles.

Suspending from vines and tree branches is one thing, but also, climbing trees with immature musculature is certainly helped by a grasping big toe.
And then of course, grasping not just trees and vines, but grasping mother is important as well.

Is there any way we can investigate this ontogeny-based hypothesis for a grasping hallux?

Let's consider the foot as a whole first, and then get back to the big toe as a grasping tool.

We can see whether foot size varies during ontogeny in different primates.

I have looked at the size of macaque (monkey), gorilla and chimpanzee (Pan) feet through ontogeny (granted, a cross-sectional sample, not a longitudinal one).***

Because macaques grow up faster than the two apes which share developmental pace, here's how I lined up the age groups (1-5; 1 = infants and 5 = adults) so that I could fairly compare growth among them.

And here are the results where I compared relative foot size during ontogeny (over age groups 1-5). Femur length was my measure for overall body size.

The box and whisker plots show you how macaques are born with big feet relative to body size, relative to adult proportions. The ontogenetic changes in proportions that they experience, over the age groups I've constructed, are significant according to the ANOVA.

By contrast, and granted I had small samples of chimp and gorilla infants ... those apes are born with adult foot size proportions which are small relative to what macaque infants are working with. Larger, more adult feet at birth contribute to macaques' relative behavioral precociality compared to young gorillas and chimpanzees who are relatively altricial. With those big feet macaques can better navigate a big world.

Chimps (and especially humans) are relatively behaviorally altricial at birth compared to macaques. Neurological development factors into this, but the small feet (in a big world) are also part of that altricial package.

Now, to bring this back around to grasping thumb-like big toes in apes!

During their longer periods of infant and juvenile dependency, gorillas and chimpanzees spend quite a bit of time clinging to mom. Big feet for body size would help cling to mother like with macaques. On a relatively small foot for body size--and in a relatively more dependent baby which is taking longer to achieve independence and is requiring more mother-infant care and bonding and learning--the thumb-like grasping big toe would come in handy (or footy).

(We've got some residual ability still...see here.)

In this scenario, the grasping hallux is an adaptation for surviving the earliest stages of life as a small footed more vulnerable, slower-developing, extensively dependent ape infant.

So what does this have to do with Pliocene hominins?

First of all, it means that morphology should be considered in an ontogenetic context so that our adaptive hypotheses and evolutionary reconstructions are as robust as possible.

And second of all, if you're basically a dedicated biped and you've got free hands to help carry your baby (rather than demand it hang on for dear life)  then selection for grasping ability in babies might be relaxed. Meaning that relaxed selection on grasping foot anatomy could have preceded any selection for all the derived features we associate with bipedalism. This isn't new territory. Most of us assume that bipedal behavior preceded the refined (as much as it can be considered refined) bipedal anatomy.

To sum up, at some point hominin infants lost the ability to cling to mother and at some point we lost our foot thumbs. These evolutionary events might be related.

What does this mean for Lucy and her kind (with their non-grasping feet) and for the Burtele foot's kind (with their foot thumbs)?

Lucy would have had to care for infants more intensely than the Burtele gang. These species would have had different mother-infant interactions.

Babyhood and motherhood...that's a whole lot more profound than straight up metatarsal anatomy.

*I was derided for not strongly-enough demonstrating claims like this in my one attempt at publishing fossil foot bone descriptions. I trust this was an oversight in moving information to the supplementary section or collateral damage due to some other editorial process. Or it's my inability to read this paper properly!
**Wunderlich (1999) measured metatarsal head pressure during walking on the ground and a pole (branch) in chimps and found that the peak pressures for MT1 were higher on the ground than on the pole. And that's not just absolutely, but relative to to the other MTs.
***Dunsworth HM. 2006. Proconsul heseloni feet from Rusinga Island, Kenya. Doctoral dissertation, Pennsylvania State University.
****Correction: should have better worded what I see as a diminished role of the grasping big toe, not the elimination of it.

"Bless the blog. Nothing else like it."

Note on the missing images: Apologies for the now dead links to once-adorable images! When I originally posted this piece, I didn't know how to best post images that could potentially disappear in the future from their source sites. 


Holly Dunsworth said...

Be my guest and swing away at the rampant adaptationism, Ken! :)

Ken Weiss said...

This is another marvelous post from your pen, Holly! It's a very fine, balanced, humerous and informative treatment.

My only reaction is that besides the difficulty of inferring function, and assuming one master function (if I can summarize a point of yours with that phrase), there is the assumption that the function was responsible for the evolutionary adaptation.

The latter, if the assumption is adaptation not as what you can do, but as what natural selection allowed you to do, then the selectionist assumption is very shaky. Because selection means some individuals have more children than others _because_ of their slightly different foot-thumb, or whatever. The case for that is much more difficult to make, I think. And you've shown that the case for function itself is a challenge.

If this isn't food for thought, than what is?

Holly Dunsworth said...

Without blogs, how did people put the minutia of their dissertation in broader terms... peppered with Forrest Gump links?

I'm thrilled to be living in the future.

Ken Weiss said...

Yes, one might say that if our chimpancestors jumped into the future feet first, we are blogging into the future head first. How will we be reconstructed from our fossil skulls?

I think that blogosphering has many very positive potentials relative to traditional media, even in science. There's a glut of etherized material, but there's also a glut of 'published' research, and I wonder if the former isn't as likely to be influential as the stodgy old traditional way. At least, if the ethersphere material stays available.

Let's see, there was the stone age, then the iron age, then the bronze age, then the atomic age, and next.....the Google age....

Holly Dunsworth said...

Thanks so much for an enlightened friend for passing this comment to me: "The fourth MT of the Burtele foot doesn't have ape-like torsion. If it did, it is an ape. It has lateral torsion, which is the human and monkey condition."

occamseraser said...

...and the metatarsal robusticity sequence of the Burtele foot isn't like that of modern humans (or OH8). Curious, eh?

Holly Dunsworth said...

I've got renewed passion about my dissertation. Both the ontogenetic and the cross-sectional geometry studies. If only I knew of a willing collaborator who has the same data on humans!

Ken Weiss said...

I'll collaborate with you! I have feet--human, and two of them (replicate observations!). I can walk, climb (sort of), run, jump, and sit back and put my feet up to relax (maybe the latter is why feet evolved). I must admit, though, that I'm not a baby (even if some think I act that way).

So I will join the study, so long as I don't have to be dead first.

Holly Dunsworth said...

Days after posting this, my curiosity still grows as to why the title calls this find a "hominin."

It's not clear at all that it is a hominin, yet the question was hardly even raised! I don't see how this isn't a Nature paper even without it being a "hominin." So I'm baffled.

Does it have to be a hominin because Ardi, with which it shared similarities, was published as a hominin?

Holly Dunsworth said...

thanks Ken!

Ken Weiss said...

Juliet had the answer: a hominin by any other name would smell as feet.

Holly Dunsworth said...

ha! A quaintessential Ken response indeed!

Holly Dunsworth said...

I'm also regretting that fossils like this weren't around when I wrote my dissertation proposals for funding. I could have TOTALLY justified collecting human and hominin fossil data. Alas, back then Proconsul was not as sexy as it is now... featured in the Ardi and the Burtele papers! Primitive apes, well-preserved primitive apes to boot, are informative.

Ken Weiss said...

Well, Holly, speaking of feet, don't kick yourself over that. Everyone can always find something that, had it been known, could have been used to get funding. You have to keep looking the same direction your (human) hallux points--forward.

And, if you don't think you'll ever have another good idea, or contribution to make, then shed some tears of regret....and start driving a cab instead.

I mean, was Proconsul even sexy? I don't remember if it had any descendants to examine to see if the human shoes fit, so to speak.

Holly Dunsworth said...

haha! Thanks Ken.

BTW, the main conclusion of my diss:

Proconsul wore black platform stiletto knee high leather boots.

Ken Weiss said...

Was Proconsul a 'she'....or are you implying something more subtle about behavior in those days?

S. Abbas Raza said...

Hi Holly,

You've won third place (the much-coveted Charm Quark) in the 3QD Science Prize 2012 (and the $200 that goes with it). Please email me. :)

And congratulations!