morphometrics

I just read the new paper by Philipp Gunz and colleagues, titled, "Early modern human diversity suggests subdivided population structure and a complex out-of-Africa scenario". That's a mouthful.

The late Middle Pleistocene population of Africa was genetically variable, and that genetic variability is probably the biggest component of genetic variation still remaining in living humans. Moreover, the phenotypic variability of the Levantine sample has been recognized since its initial description by McCown and Keith (1939). So to read this is not surprising:

Seemingly ancient contributions to the modern human gene pool (36) have been explained by admixture with archaic forms of Homo, e.g., Neanderthals. Although we cannot rule out such admixture (37), the clear morphological distinction between AMH and archaic forms of Homo in the light of the proposed ancestral population structure of early AMH to us suggests another underestimated possibility: the genetic exchange between subdivided populations of early AMH as a potential source for ‘‘ancient’’ contributions to the modern human gene pool (9, 36).

I've stressed the importance of African population structure before (e.g., Hawks et al. 2008). So I agree completely with this part of the interpretation in the paper: African variation was larger than in other regions, and it was important.

But that being said, these morphometric comparisons are not very straightforward. Some comments:

1. Phenotypic variance is not a measure of genetic variance. If we see a population that has a large measure of phenotypic variability, it does not mean that the population had much genetic variability. Perversely, genetic variability can sometimes be lower in a population that has greater phenotypic variance -- often because genetic drift can cause a loss of epistases that once constrained the phenotype. In some cases environmental variance may actually increase when the additive genetic variance declines, because of a loss of developmental robusticity. In any event, we can't just go from a variable phenotype and infer that there's variation in genotypes.

2. There's no evidence for subdivision here. They measure a high phenotypic variance within the sample they refer to early modern humans. But that variance is expressed not mainly between geographic locations in the sample, but within them. Qafzeh 6 and 9 are far apart; Jebel Irhoud 2 and Skhul 5 are close together. The East African fossils Omo 2 and LH 18 are far apart. This isn't subdivision, it's just high within-population variance.

3. Weird sample composition. The early modern human sample includes the African and Levantine crania complete enough for analysis. But why lump these? Why is the South African Fish Hoek skull lumped with Upper Paleolithic Europeans?

4. Temporal range. There are two samples here that have a high average distance between nearest neighbors in the sample: "archaic" humans and early modern ones. What these two samples have in common is that they each cover a much larger range of time than the other samples. The early modern sample spans more than 100,000 years by current dates. That's more 80,000 years longer than the Upper Paleolithic sample, 50,000 years longer than the Neandertal sample -- a huge component of variance that is uncontrolled in the other samples.

5. Principal components. PC axes are those that account for the largest covariances in the sample. If two samples are lumped together, there is a within-population component of variance and a between-population component. These may be partly independent in their effects on the total variance, or they may not be. In any event, if we derive the PC structure from the total sample, or even from the individual samples pooled together, the larger samples will weight the PC structure more toward the factors that explain their within-sample covariances. In this case, we have many more recent humans than fossil ones, and many more archaic humans and Neandertals than "early modern" humans. It's hard to have an intuitive idea about the biases that can result from sample composition, and that's a big reason for caution.

Those are all reasons for re-examining the results in different ways. In particular, if I were doing this kind of analysis, I would repeat it for subsets of the cranium, where I could include a larger number of fragmentary fossils. If the African-Levantine sample is really unusually variable, that should hold up strongly when we examine parts as well as the whole cranium.

Well, although I listed several reasons for caution, we can ask how to interpret the study's conclusion:

Any model consistent with our data requires a more dynamic scenario and a more complex population structure than the one implied by the classic Out-of-Africa model.

If we take the high variance of their "early modern" sample at face value, what we have to conclude is that later humans evolved substantially less phenotypic variance than African-West Asian people who lived between 200,000 and 90,000 years ago. Genetics tells us that there was no massive genetic drift during the time span after 90,000 years ago within Africa. Thus we must conclude that some other force resulted in a significant restriction of the phenotypic variation of recent humans, including people who lived as long as 40,000 years ago.

My hypothesis would be natural selection on some significant subset of phenotypic characters, which reduced the phenotypic variance of most of the cranium by pleiotropy. An out-of-Africa migration is not sufficient to explain the reduction in variance, because all modern humans are limited in phenotypic variance, not only non-Africans. Selection on some significant set of genes would help to explain why the ancestral African population predominated within the last 100,000 years. This selection would have predated most of the recent acceleration we observe in the genomic variation of current populations -- indeed, whatever set of genes was strongly selected before 50,000 years ago might have been fixed long ago.

A wave of selection can promote dispersal and demographic growth without the necessity of complete population replacement (cf. Eswaran 2002). A substantial transition in the genetic background would alter the phenotypic effects of any genes that remained in non-Africans from their local ancestors. In other words, the answer about what happened to fossil humans outside of Africa depends on the kind of events that happened inside Africa. So from that perspective, this research is very interesting.

References:

Gunz P, Bookstein FL, Mitteroecker P, Stadlmayr A, Seidler H, Weber GW. 2009. Early modern human diversity suggests subdivided population structure and a complex out-of-Africa scenario. Proc Nat Acad Sci USA (early online) doi:10.1073/pnas.0909160106

Eswaran V. 2002. A diffusion wave out of Africa: the mechanism of the modern human revolution? Curr Anthropol 43:749-774.

McCown TD, Keith A. 1939. The Stone Age Man of Mount Carmel: The fossil human remains from the Levalloiso-Mousterian. Clarendon Press, Oxford.

Patel (2005) examines the morphology of the proximal radius in different species of apes. He sets the work into the context of earlier work on hominid positional behavior and locomotion based on the radius; in particular, the work by Richmond and Strait (2000) suggesting knuckle-walking adaptations for early hominid distal radii. A question arising from this work is whether radial morphology specifically indicates functional correlates such as knuckle-walking or climbing, or whether instead it is more generalized in its anatomy. However, the proximal radius reflects not the wrist joint but the elbow, and may not be expected to reflect the same locomotor or positional constraints as the distal end.

The analyses are admirably complex. My favorite is the one where a ball bearing is allowed to roll freely in the proximal fovea in order to measure its shape.

But the results show that the proximal radius is not a strong indicator of function:

[W]hen hylobatids were included in the comparative analysis, they were not clearly distinguishable from African apes, and early hominins resembled both African apes and hylobatids. Because African apes and hylobatids have different locomotor behaviors (see Tuttle 1986; Fleagle 1999), the results of this study suggest that determining specific locomotor behaviors from the proximal radius may not be possible -- it cannot be determined whether the bony morphology is indicative of terrestrial quadrupedal locomotion or acrobatic suspensory behaviors (i.e. brachiation). Thus, with reference to the proximal radius, it is difficult to determine whether early hominins may have had the ability to utilize any form of terrestrial locomotion similar to extant African apes, a conclusion that is similar to those of previous studies of the distal humerus (Feldesman 1982; Senut and Tardieu 1985) and proximal ulna (Aiello et al. 1999) (Patel 2005:426, references therein).

Patel does draw a contrast between monkey-like quadrupedalism and potential suspensory locomotion for the elbow joint:

Although most early Miocene hominoids [or proconsuloids (e.g. Harrison 2002)], such as Proconsul, Afropithecus, and Turkanapithecus, were quadrupedal, with a monkeylike elbow morphology (Napier and Davis 1959; Fleagle 1983; Rose 1988; 1993b; 1994; 1997; Richmond et al. 1998), the elbow region of later hominoid taxa, such as Oreopithecus, Dryopithecus, and Sivapithecus, resemble both African apes and hylobatids. This suggests that these taxa may have utilized suspensory behaviors (e.g., Begun 1992; Rose 1993b; 1997; Richmond et al. 1998) (Patel 2005:428, references therein).

This places emphasis on the question of the evolution of suspensory posture. It is quite clear that early hominoids that are probable relatives of both Asian apes and the European and African clade of apes were suspensory, such as Dryopithecus and Pierolapithecus. Gibbons are obviously also suspensory. Were the common ancestors of all living hominoids suspensory, or were they independently derived from Proconsul-like quadrupeds?

What is unsatisfying about this study is the lack of biomechanics. Consider the following:

African apes and hylobatids have relatively small radial foveae resulting from an expanded proximal articular surface. A smaller fovea results in a smaller area of contact between the radius and the capitulum, indicating an emphasis on stability (e.g. Godfrey et al. 1991).... Although the depth and the curvature of the radial fovea were not measured in this study, it would be expected that the fovea in African apes and hylobatids would be deeper and more curved to promote increased stability in the elbow joint (e.g., Hamrick 1996) (Patel 2005:429, references therein).

Why? How does the specific form of this joint promote stability? What is the contrary force making stability less desirable in species with less extensive bony articular surfaces? Patel notes that it is a bit of a mystery why orangutans should not have proximal radii more like the other apes and speculates that they accentuate mobility rather than stability. Is this true? Are chimpanzee elbow joints less mobile than humans? Are gibbons really like the African apes in function, or is there an allometric difference that leads to the appearance of similarity between them? Gorillas, chimpanzees, and orangutans are different on average, but there is overlap in some features. Do individuals in this overlap region have similar biomechanical properties, and if so, why does this degree of variability persist?

Answering these questions requires proper biomechanical modeling. One must explore the relationship between radius shape and forces acting on the elbow joint. Statistical comparisons of similarity among hominoid species are interesting, but they do not replace this process.

References:

Patel BA. 2005. The hominoid proximal radius: re-interpreting locomotor behaviors in early hominins. J Hum Evol 48:415-432.

Ackermann and Cheverud (2004) consider the pattern of selection necessary to change a nonrobust australopithecine cranium (i.e. Sts 5) into a robust australopithecine or early Homo cranium. To do this, they measure seven fossil specimens (KNM-ER 1470, KNM-ER 1813, KNM-ER 3733, KNM-ER 406, KNM-WT 17000, SK 48, and Sts 5), taking eight linear measurements on each (nasion-nasale, nasion-frontomalare, nasale-anterior nasal spine, anterior nasal spine-intradentale superior, anterior nasal spine-zygomaxillare superior, frontal-maxillary nasal suture point-zygomaxillare superior, and zygomaxillare superior-frontomalare). These are all facial measurements, so the question is the degree to which gross facial dimensions change over time.

They also have samples of humans, chimpanzees, and gorillas to provide a model of within-population facial variation. These comparative samples are used as follows:

Phenotypic within-population V/CV matrices for the facial variables from all three living primate populations were obtained by using the residual CV matrix from a multiple ANOVA with the eight traits as the dependent variables and subspecies as the independent variable, thus pooling the CV across subspecies, and were then simplified to their principal components (PCs). The PCs of the within-population V/CV matrix are ordered by their level of V (eigenvalues) and are uncorrelated with one another so that on the scale of the PCs, the within-population V/CV martix is a simple diagonal matrix with no CVs among components. PC scores are calculated for each fossil population by multiplying trait means by the standardized within-population PC loadings. The between-population V for each PC can then be calculated as the V among these population mean PC scores; these values are given in Table 2 along with the within-population Vs (eigenvalues) for each extant model (Ackermann and Cheverud 2004:17947).

I had to read that through a few times before I got it, and since I'll surely forget it, I quoted it verbatim.

From the values for each group, the amount of morphological change is estimated between the hominid populations. Random drift is expected to cause evolutionary divergence between populations in a way that is proportional to the within-population variation of traits. In other words, traits that are highly variable within populations should also vary highly between populations, and two traits that are correlated within populations should both vary in the same way between populations. By examining the PC scores within populations, they eliminate the correlations, and can consider whether the within and between-population differences are linearly related. Under the hypothesis of genetic drift, the slope of a regression between the two should be 1.0. Greater divergence time increases the expected between-population difference, but the relation with within-population variance of each trait should remain linear and with a slope of 1.0 (17948).

Since these are PC scores, it is hard for me to figure out quite what deviations from this model would mean. For example, there is undoubtedly variation about the regression line, but how much variation is too much to be consistent with the model? If the slope deviates from 1.0, that means that the high variance traits are either significantly more or less different than they should be, or the low variance traits are significantly higher in between-variation difference than they should be (they would seem unlikely to be lower than expected). And are the PC's drawn from living hominoid populations really applicable to the fossils? After all, the three contemporary species generate different PC's, and the fossil taxa are analyzed three different ways here as a result. Does the significant result in the robust australopithecines mean that they really were subject to selection, or that they fit the pattern of variation in living hominoids poorly? Since these variances are pooled into classes (australopiths, robusts, Homo), it is hard to tell.

The hominid data seem difficult to shoehorn into Lande's (1976) predictions about drift. The expectation for the degree of change over time for a trait within a population is no change. In an infinitely large set of populations, the degree of change in a single trait is expected to be distributed normally, with a variance determined by the within-population variance of the trait. What that means is that if there are a large set of populations that have diverged simultaneously from a common ancestor, the degree of variance among those populations should be predicted by the degree of variance within the populations. But for the early hominids we do not have a large range of populations; we have a set of pairwise contrasts. I should also mention that we do not have a sample of species means; we have a sample of individuals drawn from species at different times and places. For example, the "australopith" class equals the "robust" class plus Sts 5. Together, all this should mean that the scatter plot of between-population difference against within-population variance should be exactly that--a scatter.

For the significant results, Ackermann and Cheverud (2004) estimate the degree of selection necessary on each linear measurement to create the observed amount of change. These values are smoothed across a map of the face to create a graphic picture of selection intensity. This is not a real quantification of selection in terms of deaths, since each measure used here may really be linked to one or more correlated traits that affect mortality in early hominid populations.

Their results indicate that robust australopithecines emerged through a selective process operating on the shape of the upper and lower face, while early Homo did not exhibit a significant divergence from the predictions of genetic drift among the specimens sampled. They describe this result (17951):

[A]lthough the initial divergence of Homo from the australopiths may have involved selection, divergence after this time (at least in the facial characters analyzed) could have occurred through random processes alone. In other words, much of the facial diversity seen in the Homo lineage from ~2.5 million to 1 million years ago may result from random evolutionary processes, rather than adaptive evolution. Other studies have shown that craniofacial diversity in most populations of modern humans can be explained by random processes. Lynch (1990) suggests that the development of cultural inheritance could have released many of the morphological traits of humans from the pressures of stabilizing selection. This study supports that idea and supplies it with a temporal context, potentially providing direct biological evidence of a shift early on in this lineage toward nonbiological adaptation (i.e., culture) as early hominins increasingly relied on technology. Because drift tends to play a larger role in shaping diversity when populations are finite, these results also may reflect a demographic revolution toward increasingly isolated and widespread populations.

The time range cited here is probably overstating matters, considering their sample of 3 specimens. Indeed, the great size disparity among the early Homo fossils used here may have some effect on the results. I would posit that it is not time yet to accept the null hypothesis of drift, considering the failure to detect the fairly profound selection on size among the specimens. The fact that the variation among these specimens correlates linearly with the variation within the comparative samples does not prove drift; there are a number of ways that selection on facial shape might result in such a pattern. Consider for example that the gorilla comparative model (which has the greatest degree of within-sample variation and would best match the two-specimen distance of KNM-ER 1470 and KNM-ER 1813) yields a regression for the early Homo sample with an R² of 0.01. In other words, the scatter is super-high, and doesn't really prove or disprove anything. The chimpanzee and human models are very close to a slope of 1.0, and have less scatter; but their variance is arguably a worse model for early Homo including H. habilis.

For the robust australopithecines, Wood and Lieberman (2001) found that the traits that vary most within the lineage are those that are related to masticatory strain; the fact that these characters are much less variable between robust taxa (indicated by the very low regression slope found in this study) is not especially surprising: this would seem to indicate strong stabilizing selection on variable characters within taxa rather than directional selection on robust facial morphology over time.

I think a stronger study would control better by sample, with larger samples compared to each other and specific evolutionary hypotheses being tested (for example, are all early Homo erectus specimens, including Dmanisi, significantly divergent from Homo habilis?). I won't say that more features should be added, because until there are more specimens, there is no point whatsoever in adding features from a statistical point of view. Indeed, more focused questions might require that variable number be reduced. A resampling test that could determine if a very small number of traits are consistent with drift would be useful here. Even if this were simply a test of the regression, it might be handy, but especially if it tested drift directly without recourse to a regression. In particular, if such a test could directly compare pairs of species samples instead of variance within multiple-species samples, it would be a more useful test.

References:

Ackermann RR and Cheverud JM. 2004. Detecting genetic drift versus selection in human evolution. Proc Natl Acad Sci U S A 101:17946-17951.