Looking over a Neandertal's shoulder

A study by Di Vincenzo, Steven Churchill and Giorgio Manzi has fallen into the early drawer of the Journal of Human Evolution: "The Vindija Neanderthal scapular glenoid fossa: Comparative shape analysis suggests evo-devo changes among Neanderthals" [1]. The authors do a very nice job taking a long-studied anatomical feature and reframing its variation within a new context. Reading through its discussion, I find much to like in the way Di Vincenzo and colleagues deal with the variation of late Neandertals and integrate the concept of introgressive gene flow among Late Pleistocene populations.

The glenoid fossa is the part of the scapula that articulates with the head of the humerus. It's the base of the "socket" in the ball-and-socket joint of the shoulder -- indeed, "glenoid" comes from the Greek word for "socket". Roughly shaped like a rounded teardrop, the glenoid is narrower in early hominins and relatively broad in recent people. Neandertals have an intermediate form compared to earlier and later humans.

Figure 1 from Di Vincenzo et al [1]. Original caption: "The scapular fragment VI-209 and its stratigraphic position (arrow) within the Mousterian layers of complex G of Vindija cave (left) according to Malez et al. (1980). On the right, the configuration of the 60 semi-landmarks used in the analysis is superimposed on the SGF profile. Sliding points are filled. The stratigraphic column is from Janković et al. (2006). Photograph by Milford H. Wolpoff."

The main point of the study is that the Vindija glenoid specimen, Vi-209, has a more humanlike form than other Neandertals. Another conclusion based on the comparative sample is that the sample of glenoids from late Neandertals is intermediate between early Neandertals and recent people. Likewise, Upper Paleolithic and Mesolithic-era European specimens are intermediate between late Neandertals and recent people. Here's a graph with the first and second principal components of the variation; I've highlighted these groups.

Figure 2a from Di Vincenzo et al. [1]. Altered to include sample names: Krapina, "Classic" and West Asian Neandertals, Vi-209, and Upper Paleolithic/Mesolithic. X-axis is the first principal component of variation based on analysis of the whole sample, Y-axis the second principal component.

The first principal component basically depends on the relative breadth of the glenoid fossa, with living people being much broader and Australopithecus (represented by Sterkfontein Sts 7 and Malapa MH2) being much narrower relative to the overall size of the fossa. The authors tested and rejected the hypothesis that the apparent trend could be a simple effect of size. This test was carried out relative to glenoid size, and since Australopithecus had relatively large shoulders compared to Homo, size does not vary much across the hominin sample. It would be useful to consider whether body size might matter, but body size would not by itself explain the relations of the later members of the genus Homo.

The authors emphasize that the data are consistent with a single evolutionary trend within the genus Homo, so that the Neandertal-human difference should be interpreted within the context of this broader pattern. They propose a specific developmental hypothesis.

Therefore, it seems reasonable that heterochronic factors related to the prolonged developmental pattern of our species (Smith et al., 2007a), which contrasts with the faster growth rates of Neanderthals and other ‘archaic’ hominins (Smith et al., 2007b; but see; Guatelli-Steinberg et al., 2005), led to longer periods of bone deposition along the inferior-lateral edge of the SGF [scapular glenoid fossa]. This could explain the observed variation along PC1 (and/or CV1) for different morphs of the genus Homo, reaching in H. sapiens the greatest extent in width of the SGF and, particularly, of its scapular portion. This is also consistent with the observation by Churchill and Trinkaus (1990) that much of the variability of the glenoid surface is a function of size variation of the joint itself, which can be viewed as forming a single functional matrix sensu Moss and Young (1960). Thus, the overall reduction in developmental rates in the genus Homo (relative to those of other hominoids) across the Pleistocene may account for the general evolutionary trend in SGF shape seen in the fossils, with more marked changes in developmental rates between archaic (including Neanderthals) and early modern humans, producing somewhat more dramatic differences between these groups in joint shape. Green et al. (2010) suggest that some of the differences between Neanderthals and modern humans in shoulder and thoracic morphology (particularly those related to clavicular length) are attributable to differences in the RUNX2/CBFA1 gene. The temporal pattern observed here would suggest that, with respect to SGF shape at least, that some differences are due to overall differences in developmental schedules (rather than specific differences in genes controlling development of the shoulder, such as RUNX2/CBFA1 or HoxC6).

By suggesting at least one actual genetic substitution in recent humans, they lend some plausibility to the idea. I am more hesitant to accept the assumption that Neandertals had faster developmental schedules than recent people, although it could be true. This specific assumption is not necessary to support the idea of heterochronic change in the glenoid, which could be caused by much more focused developmental processes. If glenoid shape reflects heterochronic developmental changes, the data suggest that those changes were ongoing in global populations during the Holocene. Indeed, the difference between recent people in the study and Upper Paleolithic Europeans is as great as the difference between late Neandertals and Upper Paleolithic Europeans. The study's recent human sample covers a broad geographic distribution but is relatively small in numbers; a fuller comparison of recent people might uncover a more interesting pattern of change.

The scapula has long figured in discussions of Neandertal genetic persistence. Neandertal scapulae often have a sulcus (groove) on the dorsal (back) aspect of the axillary border, and this feature is also found in a high fraction of early Upper Paleolithic skeletons [2] The axillary border morphology probably has no functional or developmental correlation with the glenoid morphology, so these features are best viewed as separate issues. I mention the axillary border only because of one significant commonality with the glenoid as considered here: We don't know how much variation in the trait may be explained by environment. Maybe the way an individual uses her arms when growing will affect the form of the scapula? With the axillary border, this question has occupied many researchers who tried to determine why some humans resemble some Neandertals and vice versa [3]. The current consensus is that a dorsal axillary sulcus probably reflects early developmental processes that are substantially influenced by genetics instead of shoulder activity pattern, but the consensus is not without detractors.

In this study, the authors consider the role of introgressive gene flow among Pleistocene populations as a way to maintain the apparently continuous trend:

The morphology of the SGF [scapular glenoid fossa] is unlikely to be under the genetic control of a single locus. Thus, it is more likely that regulatory genes controlling developmental rates overall produce pleiotropic effects throughout the skeleton. The introduction of these and other (non-regulatory) alleles into the Neanderthal populations of the Near East, and their movement by gene flow across Neanderthal demes into southern Europe (well in advance of the actual in-migration of modern humans) could account for mosaic morphology seen in the Vindija G3 Neanderthals, including the Vi-209 scapula. Introgression and subsequent gene flow would not be expected to have affected early Neanderthal populations (those predating the admixture), nor late Neanderthal populations from western (trans-Alpine) Europe, because they were separated by geographic barriers ( [Fabre et al., 2009] and [Degioanni et al., 2011] ), and/or protected from gene flow by distance (as hypothesized by Voisin, 2006).

There is as yet no evidence that the Vindija Neandertal genomes have genetic introgression from the African populations from which present non-Africans derive most of their genetic heritage. Green and colleagues [4] tested explicitly for this kind of gene flow, from "modern" into Neandertal populations and found none.

And yet, the latest Neandertals are consistently similar to recent people in ways that earlier Neandertals were not. The glenoid fossa of Vi-209 is not an isolated case, it joins many other characteristics in this sample (as noted in the quote above) and other Neandertal samples after 45,000 years ago.

Frankly, I expect that the admixture estimates presented thus far will prove to be wrong. I could be wrong in this expectation, but there are many assumptions underlying genetic analyses of admixture, and it's easy for an incorrect assumption to give rise to an incorrect conclusion. I take the morphological evidence very seriously as a possible "reality-check" about the validity of genetic comparisons. After all, the morphological comparisons predicted introgression from Neandertals in the first place...

Another reaction to the study by Zachary Cofran: "Evo-devo of the human shoulder?"

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).

I think Cofran takes this in an interesting direction with respect to his own dissertation work on development in earlier hominins.

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