scapula

Evo-devo of the human shoulder?

/ zcofran / 1 Comment

It’s a new year, and while my mind should be marred by a hangover, instead all I can think about are fossils and scapulas.


A pretty cool study was published online in the Journal of Human Evolution last week, and I’ve finally gotten to peruse it. Fabio Di Vincenzo and colleagues analyzed the shape of the outline of the glenoid fossa on the scapula (not to be confused with the glenoid on your skull), from Australopithecus africanus to present day humans. The glenoid fossa is essentially the socket in the ball-and-socket joint of your shoulder. The authors found that there is pretty much a single trend of glenoid shape change from Australopithecus through the evolution of the genus Homo: from the fairly narrow joint in Australopithecus africanus and A. sediba, to the relatively wide joint in recent humans. The overall size and shape of the joint influences/reflects shoulder mobility, so presumably this shape change hints that more front-to-back arm motions became more important through the course of human evolution (authors suggest throwing in humans from the Late Pleistocene onward).



The finding of a single predominant trend in glenoid shape evolution is pretty interesting. On top of that, the authors add an ‘evo-devo’ twist by comparing species’ average “shapes” (first principle component scores, on the y-axis in the figure at right) with their estimated ages at skeletal maturity (which appears scaled to the modern human value, on the x-axis). Though it’s not an ideal dataset for running a linear regression, the figure at right shows that there appears to be a fairly linear relationship across human evolution, such that groups with an older age at skeletal maturity tend to have a more rounded (modern human-like) glenoid fossa (note that the individuals in the analysis were all adults). Overall size does not contribute to shape variation among these glenoids.


This work raises two issues, and ultimately leads to a testable evo-devo hypothesis. The first issue is to what extent we can trust their estimates of age at skeletal maturity. These estimates were allegedly taken from a chapter by Helmut Hemmer (2007) in the prohibitively expensive Handbook of Paleoanthropology. Cursorily glancing at this chapter, I can’t find age at skeletal maturation estimated for any hominids. It is possible that in my skimming I missed the estimates, or alternatively that Di Vincenzo and colleagues misinterpreted another variable as skeletal development. Either way, these estimates would still need to be taken with a grain of salt, given that it is almost impossible to know the true age at death of a fossil (but see Antoine et al. 2008), especially if there are no associated cranio-dental elements.


That said, it is perfectly reasonable to suppose that the age at skeletal maturation has increased over the course of human evolution; life-span increased through human evolution, and so all else being equal (which it almost certainly isn’t) we could expect that maturation would occur later over time, too. So this leads to a second issue: given the “evo-devo change” the authors hypothesize, what is the evo-devo mechanism? That is, how was development modified to effect the evolutionary changes we see in the hominid scapula? Because they found adult glenoid shape correlates with estimated age at skeletal maturity, this leads to the hypothesis that postnatal skeletal growth accounts for the shape difference. Indeed, they state:

“If functional and static allometric influences are unlikely, we…interpret the trend…as reflecting growth and developmental factors. A major, albeit gradual, trend of ontogenetic heterochrony occurred in the evolution of the genus Homo… and thus differences within and between taxa in overall growth rates may have produced the pattern of variation between samples, as well as the overall temporal trend observed. The regression of life history variables [they only looked at 1]… with PCA [principle components analysis] scores supports this ‘ontogenetic’ hypothesis.”

The authors suggest that humans’ slower growth rates but longer growth period “led to longer periods of bone deposition along the inferior-lateral edge of the [glenoid fossa]”  The heterochronic process they suggest is “peramorphosis” – the descendant reaches a shape that is ‘beyond’ that of the ancestor.

The figure above is from a seminal “heterochrony” paper by Pere Alberch and colleagues (1979), portraying how peramorphosis can occur. In each, the y-axis represents shape and the x-axis is age. A the descendant’s peramorphic shape (“Ya”) could result from accelerated growth (left graph) or from an extension of growth to later ages than in the ancestor (right graph).


And so this leads to a testable hypothesis. Di Vincenzo and colleagues cite (dental) evidence that humans’ overall body growth rates are slower than earlier hominids’, undermining the hypothesis that acceleration is responsible for humans’ glenoid peramorphosis. Rather, they hypothesize that humans’ slower growth rates coupled with a longer period of skeletal development, to result in a relatively wider glenoid, due to increased development of the secondary growth centers (e.g. the graph at right, above). This developmental scenario predicts that subadult human glenoids should resemble earlier hominid adults’, that “ontogeny recapitulates phylogeny” as far as glenoid shape is concerned. Analyzing glenoid growth can even be extended to include fossils – the >3 million year old human ancestor Australopithecus afarensis has glenoids preserved for an infant (DIK-VP-1; Alemseged et al. 2006) and 2 adults (AL 288 “Lucy” and KSD-VP-1; Johanson et al. 1982, Haile-Selassie et al. 2010). An alternate hypothesis is that species’ distinct glenoid shapes are established early during life (i.e. in utero), and/or that no simple heterochronic process is involved.


ResearchBlogging.orgDi Vincenzo’s and colleagues’ study points to the importance of development in understanding human evolution, and their hypothesized “evo-devo change” in glenoid shape is ripe for testing.


References
Pere Alberch, Stephen Jay Gould, George F. Oster, & David B. Wake (1979). Size and shape in ontogeny and phylogeny Paleobiology, 5 (3), 296-317


Alemseged, Z., Spoor, F., Kimbel, W., Bobe, R., Geraads, D., Reed, D., & Wynn, J. (2006). A juvenile early hominin skeleton from Dikika, Ethiopia Nature, 443 (7109), 296-301 DOI: 10.1038/nature05047


Antoine, D., Hillson, S., & Dean, M. (2009). The developmental clock of dental enamel: a test for the periodicity of prism cross-striations in modern humans and an evaluation of the most likely sources of error in histological studies of this kind Journal of Anatomy, 214 (1), 45-55 DOI: 10.1111/j.1469-7580.2008.01010.x


Di Vincenzo, F., Churchill, S., & Manzi, G. (2011). The Vindija Neanderthal scapular glenoid fossa: Comparative shape analysis suggests evo-devo changes among Neanderthals Journal of Human Evolution DOI: 10.1016/j.jhevol.2011.11.010


Haile-Selassie, Y., Latimer, B., Alene, M., Deino, A., Gibert, L., Melillo, S., Saylor, B., Scott, G., & Lovejoy, C. (2010). An early Australopithecus afarensis postcranium from Woranso-Mille, Ethiopia Proceedings of the National Academy of Sciences, 107 (27), 12121-12126 DOI: 10.1073/pnas.1004527107


Hemmer, Helmut (2007). Estimation of Basic Life History Data of Fossil Hominoids Handbook of Paleoanthropology, 587-619 DOI: 10.1007/978-3-540-33761-4_19


Johanson, D., Lovejoy, C., Kimbel, W., White, T., Ward, S., Bush, M., Latimer, B., & Coppens, Y. (1982). Morphology of the Pliocene partial hominid skeleton (A.L. 288-1) from the Hadar formation, Ethiopia American Journal of Physical Anthropology, 57, 403-451 DOI: 10.1002/ajpa.1330570403

"Big Man" and the scapula of Australopithecus afarensis

/ zcofran / 2 Comments

Last November I reported on recently described Australopithecus cf. afarensis craniodental remains from the site of Woranso Mille in Ethiopia. These fossils are significant in part because they date to around 3.6 million years ago; most of the postcranial evidence for A. afarensis comes from Hadar (~3.4 – 2.9 million years) or Maka (~3.5 million years). It is pretty awesome, then, that Yohannes Haile-Selassie and colleagues (2010a) have just reported on a partial skeleton from Woranso-Mille.


The specimen is given the catalog number KSD-VP-1/1 (right, from Nature), and the nickname Kadanuumuu, meaning “Big Man” in the language of the Afar people who live in the region where the fossils were discovered. Here, I’ll be focusing on the scapula.

Researchers have debated about what the scapular form of A. afarensis means functionally – how could, and did, these creatures use their shoulders? The scapula of AL 288 (the famous “Lucy”) preserves part of the glenoid fossa (shoulder socket) and only a little of the surrounding bone including the scapular spine (below). It has been argued that the angle between the glenoid fossa and the lateral border is more similar to modern apes than to humans. That is, the shoulder socket may have been oriented more upward, like in modern apes, compared to humans whose socket faces more to the side. The implication is that A. afarensis may have been preferentially exploiting arboreal environments.

Left: AL 288 scapular fragment. The glenoid fossa is the hollow that faces to the right, the lateral border is at the bottom paralleling the label “AL 288-1L.” The scapular spine is preserved only at the base, it is the small uprising of bone just to the left of the glenoid fossa. From Haile-Selassie et al. 2010b, Fig. S21.

Similarly, a juvenile afarensis skeleton from the Ethiopian site of Dikika (Alemseged et al. 2006), dating to around 3.4 million years ago, also suggested an ape-like shoulder for this extinct human ancestor. Principle components analysis of several measurements from the Dikika scapula showed it to be very similar to gorillas of comparable age, in terms of overall shape and proportions.

So from these two scapulae, one belonging to a very small-bodied female, the other from a small ~3-year-old possible female, we get the picture that A. afarensis had a fairly ape-like (i.e. arboreal) shoulder orientation, and may not have had independent movement of the head and trunk that we modern humans enjoy. Nevertheless, it is still unclear whether this means that the afarensis scapula functioned like that of an ape, and hence its shape, or whether the similarity in shape is a ‘hold-over’ from having an arboreal ancestor. I will say, I think one very telling feature noticeable in even the fragmentary AL 288 is the relative position and orientation of the scapular spine. Note that in the apes (the two juveniles scapulae on the right of the diagram to the left), the scapular spine roughly parallels the lateral border, and as a result, the flat areas above and below the spine are roughly equal in size. The above area houses the supraspinatus muscle, a rotator cuff muscle that acts largely in elevating the arm above the head and stabilizing the shoulder joint. In humans and afarensis, in contrast, the lower (insfraspinous) fossa is fairly large compared to the upper (supraspinous) fossa. Thus, the argument can be made that in humans and hominids, less power is needed to raise the arms over the head, or that humans and hominids have a greater reliance on the infraspinatus muscle for bringing the arm down toward the body and stabilizing the shoulder joint.

Now, KSD-VP-1 provides a remarkably complete scapula of an adult afarensis (right). In contrast to the specimens described above, KSD-VP-1 is very human-like. To the naked eye, and as borne out by principle components analysis of scapular angles, this thing is very human-like.

Now the question is, why does the morphology of this new specimen seem at odds with Lucy and Dikika? Part of the answer could be scaling – indeed, the authors note that the orientation of the glenoid relative to the lateral border (more specifically the scapular bar) in AL 288 can be found in modern humans of small size.

But that still does not answer the question of why the complete adult afarensis scapula is like adult humans, whereas the child afarensis is like young gorillas. The authors posit that perhaps it is due to Dikika’s fairly large supraspinous fossa. They also suggest that the measurements used in Alemseged et al’s study could not capture functional and discriminatory information about scapula shape. Nevertheless, a simple visual comparison the Dikika and KSD (x-ray…) scapulae reveals them to look fairly different, i.e. Dikika is relatively broader side-to-side.

Could ontogeny explain the differences between the child and adult afarensis? In a study of scapular growth and development in living primates, Young (2008) found childhood growth does not appear to explain adult shape variation. That is to say, most aspects of species-specific morphology are present in subadult scapulae. Rather, most variation in scapular shape among modern primates appears to be due to functional differences: climbers’ scapulae differ consistently from quadrupeds’. So what does that imply? That at 3.59 million years, adult male A. afarensis were not using their shoulders for arboreal activities, but at 3.4 million years ago, subadults were? Maybe this is just normal intraspecific variation? Maybe the ontogeny of the scapulae needs to be examined further?

I have to say I agree with Haile-Selassie et al. (2010a) here, that differences in the statistical analyses between the current study and that of Alemseged et al. (2006) may be partly responsible for the different interpretations of A. afarensis scapular morphology. Still, visual inspection of pictures of the fossils suggests to me that even if the principle components analyses were carried out using the same variables (Alemseged et al. used linear measurements, H-S et al. used angles), Dikika might seem gorilla-like, KSD still human-like; Nota bene that principle components analysis is not actually a test in itself, but rather an exploratory statistical technique. As such, it will never really “tell” how a bone was used. Still, I think this does raise an important issue about scapular function and ontogeny in hominoids.

References
Alemseged Z, Spoor F, Kimble WH, Bobe R, Geraads D, Reed D, and Wynn JG. 2006. A juvenile early hominin skeleton from Dikika, Ethiopia. Nature 443: 296-301.

Haile-Selassie Y, Latimer BM, Alene M, Deino AL, Gibert L, Melillo, Saylor BZ, Scott GR, and Lovejoy CO. 2010a. An early Australopithecus afarensis postcranium from Woranso-Mille, Ethiopia. Proceedings of the National Academy of Sciences, USA, in press.

Haile-Selassie et al. 2010b. Supplementary Online Material to 2010a.

Young NM. 2008. A Comparison of the ONtogeny of Shape Variation in the Anthropoid Scapula: Functional and Phylogenetic Signal. American Journal of Physical Anthropology 136: 247-264.