john hawks weblog

This post in progress...

Here are some thoughts on memetics as construed by Blackmore. The book has 18 short chapters along with a preface and a foreword by Richard Dawkins, so I do not comment on everything. Just some notes as I am reading.

I am mostly sympathetic with the concept of memes, but I retain some skepticism about the ways that the concept may or may not be applicable to human evolution, either cultural or biological. My basic thought is that it serves us little to consider the ways that memes may be structured to maximize their own dissemination and retention, but it is potentially very applicable to consider the ways that human minds may be adapted to retain or spread certain kinds of information. Thus, if a meme is a behavioral analog of a gene, then what I think is interesting is whatever would be the behavioral analog of developmental genetics--the biological evolution of an unfolding genetic program that creates a mind via interaction with a cultural environment. To what extent are minds genetically inherited (i.e. culture- or meme-independent) and to what extent are they culture- or meme-constructed?

This question may seem trite, in that it amounts to a restatement of the nature vs. nurture question. But there really isn't a way to address the biological evolution of human cultural capacities without grappling with it. If cultural capacities are largely bootstrapped by cultural learning in a substrate-neutral context, then the particular genetics underlying mind construction might matter relatively little in the emergence of modern human behaviors. In contrast, if most interesting human behaviors are culture-independent or universal, then we require explanations for them that explain their commonality in the face of cultural variation. One possibility is that culture is constrained, either logically or biologically. Another is that human cultural capacities are strongly genetically determined in some respects. It is very likely that most human capacities are in between, and in fact that the extent to which they are facilitated by particular genotypes may vary from person to person.

My thoughts also boil down to a question of the kind of variation that we consider to be interesting--culturally variable or culturally universal? For me, the question of memetics is whether memes are phenomena that have importance to the construction of minds from the perspective of biological evolution. I am reading the book with that question in mind. It could be the case that the behavioral choices that underlie survival and reproduction are highly influenced by the ease with which particular information structures may be transmitted and retained by individuals. In that case, the neurobiology that enables the replication of memes may be a relevant way to frame the issue of biological evolution. But it may be the case that the interesting ways in which memes are transmitted and maintained have no special relevance to survival and reproduction. Even so, memes might be very interesting in some intellectual pursuits, such as the analysis of changing hemlines or urban myths, but they would not constitute an interesting way to construct a theory of the evolution of cultural capacities. Again, I suspect the truth is somewhere in between these extremes, but if so there might remain some way other than memetics to make a productive theory of the origins and evolution of culture.

A few notes before starting. Here I use several terms in a way that is meant to avoid confusing myself. For this reason, they may seem idiosyncratic, but hey, it's my weblog. I use cultural evolution to refer to changes in culture over time. This has no necessary implications for the utility of cultural categories or their value to individuals, but those may be factors that affect the pattern of cultural evolution, certainly. My main interest is in the biological evolution of those mental functions that allow cultural behavior in humans and other animals. For this, I refer to the evolution of cultural capacities. With respect to the study of "capacities," it goes without saying that no two individuals are likely to be identical in performance, and in practice their manifestations of surface behaviors are likely to be very different. From a biological perspective--especially as applied to survival and reproduction--differences in performance have to be considered in a statistical framework. That is to say, do two individuals have the same likelihood of exhibiting particular behaviors in particular contexts? Could they both be expected to learn the same information given the same inputs? These are questions that focus on capacities rather than performance, and they illustrate that selection on mental capacities may occur as a function of statistical relations between minds and behavior, even if there may be no sense in which the structure of minds can be said to determine behavior.

Foreword

Dawkins originated the meme concept in his 1976 book The Selfish Gene, and as such he is certainly the best qualified to provide an introduction and contextualization of this book.

Peter Ungar (2004) investigated the dietary adaptations of A. afarensis and early Homo by looking at the three-dimensional topography of their teeth. the shapes of the teeth are expected to reflect diet because the teeth themselves are adaptations for processing food. Among mammals there are some regular relationships between the morphology of an organism's teeth and the type of food it prefers. Looking specifically at primates, high-crowned teeth that interlock between the upper and lower jaws are adapted to shearing foods, in a manner analogous to the pinking shears of a seamstress. Shearing is necessary for cutting and puncturing through food items, which are the predominant actions necessary to process leaves and insects, respectively. Primates that specialize on other foods, notably fruits or harder objects like seeds, tends to have flatter teeth without high crests. These teeth useful for crushing or grinding foods. So and examination of the anatomy of the teeth is expected to give insights about the diets of ancient primates.

But direct examination of fossil tooth anatomy is complicated by the fact that the teeth wear during the course of an animal's life. The effective chewing characteristics of a tooth therefore change over time, as a result of progressive attrition on its occlusal surface. This means that it's difficult to measure the anatomy of teeth, as in the lengths of different crests or the area of shearing surfaces, because these characteristics are altered in individuals of different ages. This is a special problem among early hominids, whose teeth are generally heavily worn even among relatively young individuals. It also means that the chewing characteristics of younger individuals and older individuals may actually have been different, possibly reflecting ontogenetic differences in diet. The details of the anatomy of unworn teeth may have been largely irrelevant to the pattern of mastication throughout most of the individual's life.

Ungar (2004) applied three-dimensional modeling to assess the shape characteristics of teeth at different stages of wear. In this way he was able to quantify the surface characteristics of the teeth--that is, how flat or jagged they were, how high the cusps were, and any angulation or deviation from a horizontal occlusal surface. He applied the technique to a series of second mandibular molars (M two) of Australopithecus afarensis and early Homo (including specimens attributed to H. erectus, H. rudolfensis, and H. habilis). As a comparison, Unger also examined a series of gorillas and chimpanzees, not because their diets were probably similar, but because their molar cusp patterns are similar, yielding comparable topographic results. The topographic values derived from each of the specimens included the "average slope," which was a measure of the average vertical displacement between adjacent points on the tooth, and the "occlusal relief," which was the measurement of the three dimensional surface area scaled to the two dimensional occlusal surface area of the tooth. In principle, more jagged teeth with higher cusps will have a higher average slope and a higher occlusal relief.

The results indicated that the early Homo specimens had relatively high average slope, except in the most worn molars. These specimens had average slope near that of gorillas, which were the highest among the samples measured. The occlusal relief of early Homo molars was not as great as that of guerrillas, but was substantially larger than chimpanzees, except again among the most worn specimens.

In contrast, A. afarensis had by far the lowest average slope and occlusal relief among any of the samples. Chimpanzees were lower than early Homo, but the A. afarensis sample was still significantly flatter in its dental morphology. These results held true across a range of wear categories, degrading slightly among the most worn sample of teeth in all four species. But as teeth wore down in all four species, they tended to become flatter. His results perhaps isn't surprising but does inform about the chewing characteristics of the teeth of older individuals.

Ungar (2004) includes a discussion that addresses why the differences in surface characteristics may have come to characterize these samples. He begins with a discussion of the differences between chimpanzees and gorillas in their diets:

The differences in occlusal morphology between chimpanzees and gorillas evidently relate to differences in the material properties of the foods they eat, particularly their fallback foods. Central African common chimpanzees are primarily frugivorous, with soft fruits reported to constitute 70-80% of their diets (Kuroda, 1992; Tutin et al., 1997). Fruit is also commonly consumed by western lowland gorillas, making up about half of the food species found in their fecal remains (Williamson et al., 1990; Nishihara, 1992; Remis, 1997; Doran et al., 2002). Differences and similarities in food preferences are most obvious were these taxa are sympatric and have access to the same resources. At Lope, Gabon, for example, the dietary overlap is substantial, with gorillas reported to consume 73% of the food species eaten by chimpanzees (Tutin and Fernandez, 1985). Differences between the two taxa are notable at times of fruit scarcity though, when gorillas fall back on tougher, more fibrous foods (such as leaves and stems) than those eaten by chimpanzees (Tutin et al., 1991; Remis, 1997) (615).

It should be reiterated that differences in occlusal morphology between P. t. troglodytes and G. g. gorilla evidently reflect differences in fallback resources rather than preferred foods. While both tax evidently prefer soft fruits when available, differences in occlusal morphology apparently allow the gorillas to take advantage of fallback foods that are less accessible to the chimpanzees (615)

For the case of A. afarensis, Ungar concludes that the differences in occlusal morphology from chimpanzees are not as great as the differences between chimpanzees and gorillas, although in the opposite direction. In his view this implies that A. afarensis included more brittle, less deformable foods, possibly as a fallback strategy in contrast to chimpanzees.

For the case of early Homo, the conclusion is that the molars were intermediate between chimpanzees and gorillas in their occlusal characteristics. This means that, compared to chimpanzees and compared to A. afarensis, early Homo was better adapted to chewing "tough, pliant foods" (616). This has important implications for dietary reconstruction in early humans:

[T]ubers, especially larger ones (Baritelle and Hyde, 1999) are often fairly brittle, whereas mammalian soft tissues tend to be tough and elastic (Lucas and Peters, 2000). Thus, meat seems more likely to have been a key tough-food resource for early Homo then would have USOs. It has also been noted that USOs those are of limited nutritional value (Schoeninger et al., 2001), and so would not have made very good keystone resources (616-617)

Ungar does not mention a number of other arguments that might also favor this interpretation. The contrast between Homo and A. afarensis is in the same direction as the contrast in occlusal morphology between primarily meat-eating carnivores like felids and canids as opposed to more omnivorous carnivores like bears. Another observation is that meat is a major food resource of chimpanzees, although this is hardly a fallback resource. Indeed, if meat eating was indeed an important component of the behavioral repertoire of early Homo, it probably is not fair to assert that the difference in diet between Homo and Australopithecus was primarily a difference in fallback resources. It may be true that australopithecines and early Homo overlapped in their food resources, particularly in plant species consumed. But considering the likely effectiveness of early humans as predators, I think it likely that the fallback foods of early humans--when hunting was ineffective--may well have been the preferred foods of australopithecines. And when australopithecines were forced to abandon their preferred foods by early humans, they were forced to fall back upon resources that either were common or were difficult for early Homo to exploit. The disappearance of early small-bodied Homo by around 1.6 million years ago, and the ultimate extinction of the robust australopithecines after a progressive increase in their molar sizes (Wood and Lieberman 2001) indicate that this fallback strategy could not be maintained in the face of increased hunting effectiveness by large-bodied Homo.

References:

Ungar P. 2004. Dental topography and diets of Australopithecus afarensis and early Homo. J Hum Evol 46:605-622.

Other references therein.

Lowell and Shulman (2005) report on the possible links between the metabolic defects underlying type 2 diabetes and mitochondrial dysfunction. These links go through two channels. In the first, decreases in mitochondrial activity in older adults were associated with higher levels of triglycerides in muscle and liver tissue as well as greater insulin resistance in muscle tissues. This observation supports the hypothesis that mitochondrial oxidation of fatty acids becomes less effective in older individuals, "which in turn lead[s] to increases in intracellular fatty acid metabolites...that disrupt insulin signalling'' (384). It is not clear whether this alteration is due to mitochondrial loss or reduction in function, but the authors suggest based on several other studies that there may be a connection with an accumulation of mtDNA mutations in elderly individuals.

The second channel involves the secretion of insulin by beta cells in the pancreas. In individuals with insulin resistance, the body can sometimes adapt to greater insulin requirements by ramping up the production of insulin in the pancreas. This pathway of insulin secretion depends on the mitochondrial metabolism of the beta cells. This connection has been established by the fact that mtDNA mutations can induce hereditary diabetes by causing beta cell dysfunctions.

Changes in fatty acid metabolism would likely be necessary at least twice during the evolution of early humans. With a dietary change toward greater meat eating, either at the origin of the habilines or that of early large-bodied Homo, a greater dietary availability of animal fats and focus on those resources might well have driven a selective change in digestive metabolism. The highly meat-dependent diet of people in the northern extremes, including the Neandertals, would have focused most digestive and metabolic resources toward animal protein and fat, and might have required additional changes. Then, a shift from a Neandertal-like diet to a broader diet during the Upper Paleolithic might well have required an additional change. It is not obvious that these shifts occurred globally, and there may well have been regional differences in meat digestion and metabolism based on local selection due to dietary differences. If the mtDNA was one of the genetic regions affected by such selection, there may well have been a very complex pattern of evolutionary changes in this molecule across the human lineage. This could account for changes within the Neandertal lineage, as well as the apparent replacement of Neandertal mtDNA by a type prevalent in recent humans.

References:

Lowell BB and Shulman GI. 2005. Mitochondrial dysfunction and Type 2 diabetes. Science 307:384-387.

This is Richard Roberts in an Australian radio interview (the interview is formatted in one-sentence paragraphs, this is a single contiguous excerpt):

Let's take a point of argument that this particular individual with a small brain is a microcephalic individual, is such an individual.

They have other features that indicate they're not suffering from microcephaly, they have unusual tooth structures - three roots to the teeth.

You find those in three-million-year-old people like Lucy in Africa, that only exist in very early Homo erectus.

You don't find those with modern humans.

We don't suddenly develop three roots to the teeth.

Nor do you suddenly develop long arms if you have microcephaly.

And that's what the hobbit has, they have slightly longer arming compared to ourselves.

The pelvis is wider than in modern humans.

They have very thick eyebrow ridges.

None of these are features of microcephaly.

When you look at a complete set of features of the skeleton, one or two of them might be credible as being microcephalic problems, but the rest of them can't be explained by microcephaly.

If you pick some of the ones like Professor Jacob has done I can understand how he reached that conclusion.

But not on the basis of all available features.

In my book, this fits the "quacks like a duck" definition of australopithecines. Nothing really new here (except a confirmation of the second jaw earlier in the interview). It's not clear to what extent these comments really reflect the biologists'; for example, LB1 has no preserved arms, and the radius from the site is not all that long.

Trawling through the original Nature article, we find these descriptions of australopithecine-like similarities.

There is a strong posterior angulation of the symphyseal axis, and the overall morphology of the symphysis is very similar to LH4 A. afarensis and unlike Zhoukoudian and Sangiran H. erectus. (Brown et al. 2004:1058)

The femur shaft does not have a pilaster, is circular in cross-section, and has cross-sectional areas of 370 mm2 at the midshaft and 359 mm2 at the midneck. It is therefore slightly more robust than the best-preserved small-bodied hominin femur of similar length (AL288-1). Distally there is a relatively high bicondylar angle of 148, which overlaps with that found in Australopithecus (1059)

.

I would add to these the prominence of the anterior superior iliac spine, and I would quadruple the weight of the brain size in the decision--I just can't see a Homo-like brain size reducing to the smallest known for any hominid as a consequence of dwarfism.

Against these, we have a number of Homo-like features.

Although LB1 has the small endocranial volume and stature evident in early australopithecines, it does not have the great postcanine tooth size, deep and prognathic facial skeleton, and masticatory adaptations common to members of this genus. (1060)

But all of these specifically Homo-like similarities are problematic, because they all are correlated with a single feature: dental reduction. And several of these features are not shared with the members of early Homo to which the specimen is proposed to be related.

The tooth sizes of the LB 1 specimen are generally shared with humans. This means, significantly, that they are not synapomorphies of early Homo--it would take nearly as much change to generate this pattern from an early Homo dentition as from an australopithecine or habiline.

I haven't made up my mind entirely, and much of my consideration runs with the brain size. Again, I would say that pathology must be rejected for the brain size before turning to other hypotheses. But the recovery of additional similar specimens would make pathology seem infinitesimally unlikely as an explanation for all of them. We aren't there yet, but we must be on the cusp of it. A divergence date from mtDNA would help a lot.

More on the Flores hominids

Hinds and colleagues (2005) report in Science on a study that involved determining the genotypes in a sample of 71 people of 1,586,383 single nucleotide polymorphisms (SNPs). The sample is drawn from Americans in three subsamples representing African, Asian, and European ancestry. The goal of the study was to add to knowledge about the frequencies of SNP variation in different medically relevant populations, while assessing the linkage among SNPs. These data would help formulate better strategies for tracing the genetic correlates of disease and other phenotypic traits.

The data were acquired with these medical goals in mind, which limits to some extent their ability to address interesting issues about human evolution. For example, they select known SNPs that were judged to be likely to be high in frequency in multiple populations. This process, called ascertainment, was complicated enough to make it difficult to use the data in models of genetic evolution. For example, a large set of the candidate SNPs were selected from public databases, which are not random representatives of the three subpopulations considered here, making it likely that the three would differ in allele frequencies in ways characteristic of this bias. Because of the ascertainment complexity, it is unlikely that geneticists would be able to use these data to accurately reconstruct ancient evolutionary events (although it may not stop them from trying).

The most interesting part is a brief consideration of the role of natural selection in differentiating populations from each other. As the authors note, one suggestion concerning the distribution of genetic differentiation (as measured by F_ST) is that different genes have undergone very different patterns of global or local selection. The suggestion from this hypothesis would be that candidate genes to examine local selection could be identified from relatively large F_ST values. (Such genes would have high F_ST in any event; the distinction is that if genetic drift were largely responsible for human differentiation, then many non-locally-adapted genes might also have high F_ST values.) As they put their findings:

If this is true, then larger F_ST values should be found near functional genetic elements. We looked at the distribution of F_ST for SNPs that were genic or nongenic, coding or noncoding, and synonymous or nonsynonymous. We performed the analysis within subsets of SNPs grouped by MAF [mean allele frequency], so that effectively, we looked at the fraction of between-population variance for SNPs with the same total genetic variance. Common SNPs in genetic regions do have slightly but significantly higher F_ST values than nongenic SNPs with the same MAF . . . and common coding SNPs have slightly higher F_ST values than noncoding SNPs in genic regions. . . . These results are consistent with local selection changing the distribution of F_ST near functional sequences. However, because the distributions of F_ST among genic and nongenic SNPs are very similar, large F_ST values by themselves appear to be very weak evidence of selection (1074).

Of course there is another reason that genic and coding SNPs might not be much more differentiated than the average: if global selection has constrained them to similar frequencies. Given the huge range of genes in the scope of this analysis, it is hard to say which force of selection should be predominant, or if they should be nearly balanced in the way they would appear to be to explain the data. Certainly genes like the MHC genes would be expected to be held at broadly similar frequencies across populations. But then some of those are precisely the genes that should be very different among populations, as a result of different microbial histories. The authors also examined the private (confined to one sample) SNPs to see if they were more likely to be genic, finding that they were not. This is not surprising, since these alleles are by definition rare, and therefore unlikely to underlie strong selected differences between populations. The few that might be locally selected are surely lost in the volume of rare alleles that are either deleterious or subject entirely to drift.

It seems to me that the way to address the F_ST issue is to examine the distribution of F_ST estimates for the SNPs. Given the observed sample frequencies of the SNPs and some assumptions about population histories, it should be possible to derive an expected distribution of F_ST. Comparing that expected distribution to the observed distribution would give some information about whether the genes had been subject to drift alone, or whether they had been significantly perturbed in some way.

The data are
publicly available; if you can think of a good use for them, have at it!

References:

Hinds DA, Stuve LL, Nilson GB, Halperin E, Eskin E, Ballinger DG, Frazer KA, and Cox DR. 2005. Whole-genome patterns of common DNA variation in three human populations. Science 307:1072-1079.
Science Online

OK, that headline looks like the title to a dissertation, which this isn't. But in honor of Mayr's recent death, I was looking through some of the things he has written about hominids, and I came across his book review of Jeffrey Schwartz's book, Sudden Origins. Reading this at once reminded me why Mayr has been such a giant in evolution that he spilled over into anthropology, and saddened me that there are so few representatives of such wisdom left.

Here are some quotes:

[Schwartz] correctly criticizes the strictly linear view of descent held by most anthropologists (p. 43), but by not thinking in terms of populations, Schwartz does not convert hominid history into a dynamic picture of the movement of geographically vicariant populations and subspecies. Such multidimensional thinking, introduced by the founders of the Evolutionary Synthesis, is not yet popular among physical anthropologists (978).

Phenotypic discontinuity does not conflict with Darwinian theory. If, for instance, a phyletic line evolves form the possession of two to the possession of three molars, the change does not occur by mutations giving one tenth, later one fifth, and one half of a new molar, but by one tenth, later one fifth, and then one half of the population having one new molar (978).

And here's rubbing it in:

What is the reason for Schwartz's failure in spite of his extensive reading and his efforts to make use of some of the most recent findings of molecular biology? Perhaps it is due to an insufficient consideration of some of the basic concepts of the synthetic theory. For instance, nowhere does he adequately emphasize that evolution takes place in populations and consists of the replacement of individuals, generation after generation. Furthermore, in numerous discussions of mutation in this volume, it is always implied that the gene (mutation) is the target of selection rather than the phenotype of the individual, and this favors acceptance of a theory of a saltational role of homeobox genes. Nor does Schwartz seem to appreciate that natural selection is a two-step process. Homeobox mutations occur during the first step, the production of variation. The fate of these mutations, after they have become components of new genotypes, however, is decided at the second step, the actual selection. Therefore, no conflict exists between the occurrence of homeobox mutations and the classical Darwinian process (979).

Consider that here, Mayr was in his early 90's. That some of us forget the lessons of the Synthesis is a discredit to us and our teachers, certainly not to the founders. Yet he patiently explains the way that today's developments in genetics should be incorporated into an evolutionary model, using the understanding that he helped the field to develop some sixty years before.

References:

Mayr E. 1999. Sudden origins (book review). BioEssays 21(11):978-979.
Wiley InterScience

The news stories (nature.com) are focusing on the idea that the "earliest" modern humans are now 35,000 years earlier than they had been. This is the amount by which the Omo Kibish specimens are now believed (McDougall et al. 2005) to be older than the previous contenders for "earliest modern humans," the 160,000 year-old Herto hominids (White et al. 2003). A bit of a discussion has been underway on the
Palanth forum as to whether the 195,000 year estimate is really warranted, or whether there is more properly considered a broader range of error.

It is important to have good stratigraphic placement and dates for the Omo Kibish specimens. Most of the Middle Pleistocene African fossils are associated only with poor dates or imperfectly known proveniences. Aside from the recent Herto sample, the dates for other important specimens are truly uncertain. So the knowledge that these hominids are broadly contemporaneous with Herto is immensely valuable.

Why are the Omo Kibish hominids considered to be modern?

This depends on one's definition of "modern humans." Many paleoanthropologists do not accept a distinction that sharply separates "modern" humans from "archaic" humans. For these scientists, the Omo Kibish specimens may simply be considered as representatives of their time and place, part of an evolutionary series leading to recent humans.

There is no question that features of recent aspect occur within the late Middle Pleistocene African sample. Especially Omo 1 has similarities in overall cranial shape with more recent people. Such similarities also may characterize its facial form, although these details are subject to the reconstruction. Taking the Omo skulls as a sample, together with the Herto sample, the full range of anatomy spans from relatively modern to substantially archaic. Here are some pocket descriptions (leaving out the child's skull BOU-VP-16/5):

• Omo 1: The occiput is rounded in profile, with only slight flattening of the parietals above lambda. In posterior view, the outline of the skull shows a maximum breadth relatively high on the parietal bones, narrowing significantly lower on the temporals toward the cranial base. The supraorbital torus is not greatly thickened even at the midline, and it thins toward the edges in a form that is continuous with the frontal squama. The interorbital space is relatively narrow. And as reconstructed, the skull appears to have both malar notches and a chin.
• Omo 2: Here, the skull is markedly more angled in the occiput than in Omo 1. The maximum breadth of the skull is at the base, across the temporals, and the sides of the skull are more or less vertical. There is a well-marked angulation of the parietal bones, meeting in a rounded keel. There is a slight angular torus on the parietal, and a well-marked nuchal torus transversely extensive across the occiput. But the frontal bone is continuous into the supraorbital region with no sulcus separating them, and the supraorbital torus itself is relatively thin laterally--perhaps as much or more so than Omo 1.
• BOU-VP-16/1 (Herto): The skull has a distinct angulation in the occiput, as great as Omo 2, with a very long nuchal plane. The skull appears to be slightly broader across the parietals than at the base, but the sides are essentially vertical: there is no distinct parietal boss. The nuchal torus is marked across the occiput, with a distinct downward-projecting inion. The browridge is moderately thick centrally, with a strong superciliary portion, and a clear sulcus dividing it from the curving frontal profile. There is a clear division between this superciliary arch and the lateral torus, which at its lateralmost extent is in the same range of thickness as the Omo 2 lateral torus. The zygomatic bone is very large, with a massive forward-facing cheek, hollowed into a canine fossa medially and malar notch inferiorly.

Several commentators have raised the issue of whether this sample contains multiple species (one going so far as to posit that the "species" immediately ancestral to our own might be preserved alongside the "modern humans" in the personage of Omo 2). A lateral comparison of the three skulls (where their comparable parts are most visible) shows that the differences are not that extensive. The Herto skull and Omo 2 are very similar in profile, with BOU-VP-16/1 being slightly higher in the forehead. Omo 1 contrasts with these in its rounded occiput, but the frontal profile of all three specimens are similar, as are their lateral torus thicknesses. Omo 1 and 2 diverge greatly in the position of their greatest cranial breadth and shape of their cranial walls; BOU-VP-16/1 is intermediate between them. All three are robust, with Omo 1 the least robust of the three. Presumably, all three are males. Their variation is extensive, but not surprising for three crania in a single region of the world.

Are they modern humans? As White and colleagues (2003) show, the Herto skull is outside the range of all recent humans in several cranial measurements. This is no doubt true for Omo 2 as well (although possibly not for Omo 1). But these are not recent, they are ancient. As a sample, they are certainly significantly different from any living sample. They are also certainly significantly different from Neandertals, and from earlier Africans.

So do we define "modern" humans in contrast with some earlier group? Or do we define them based on the variability within living people?

The answer here really is in the word "definition." If modern humans were really an evolutionary individual--a "thing" that could be discovered--then we shouldn't have to define them. We should be able to discover the boundaries of the group by examining discontinuities among fossil specimens. The fact that we have to find a definition (and that we have such trouble doing so) is in my mind sufficient to suggest that "modern" humans are not an evolutionary individual.

References:

McDougall I, Brown FH, Fleagle JG. 2005. Stratigraphic placement and age of modern humans from Kibish, Ethiopia. Nature 433:733Ð736.
Nature

White TD, Asfaw B, DeGusta D, Gilbert H, Richards GD, Suwa G, Howell FC. 2003. Pleistocene Homo sapiens from Middle Awash, Ethiopia. Nature 425:742Ð747.

Elton and colleagues (2001) examined the record of brain size in early Homo with the following question in mind: we know that brain size increased in this lineage, but was that increase unusual compared to other lineages of primates at the same time? To answer this, they examined the brain sizes in fossil A. boisei and Theropithecus (the genus that includes living gelada baboons). Answering this question would determine whether the brain size of early Homo increased for reasons unique to this genus, or whether instead it was part of a broader trend that might be attributed to climatic changes or other ecological factors.

The results of the study showed that fossil Theropithecus showed no particular trends in brain size over time. But A. boisei did show a significantly positive trend toward brain growth over time. This trend exists whether the early KNM-WT 17000 specimen is included in the sample or not, which is important because this skull is both small and early, and by itself might create a trend in a sample that was otherwise static over time. Without that skull, the trend is still there, driven mainly by the late large skull from Konso KGA 10-525, and the early small juvenile skull Omo L338y-6. Although this latter skull is juvenile, they use an estimated adult size that is about 4 percent larger than the actual endocast.

The study compared these two cases with the evidence for brain size in early Homo. Looking only at Homo habilis, there is no apparent trend toward increasing brain size. This is partly because the largest specimen, KNM-ER 1470, is early and partly because of the great variation within the sample. The overall sample including H. habilis and early humans does show a significant trend over time, but this trend appears mainly to result from the presence of two distinct (and mostly discontiguous) species, one of which survives much later in time and therefore greatly influences the appearance of a trend. Considering early humans alone, there is really no trend evident before 1.5 million years ago, and only a slight increase up to the sample around a million years ago (Lee and Wolpoff 2002).

Some issues:

The study focused on change within each fossil species. But there is no comparison to the magnitude of changes that occurred between hominid taxa. This is problematic because most of the brain evolution in early Homo likely characterized the initial origin of the lineage from an ancestral australopithecine. It is no great surprise that H. habilis does not change markedly over time, but what is surprising is the substantial jump in size from earlier australopithecines like A. afarensis or A. africanus and later Homo. The same could be observed of the change between habilines and early humans. The authors actually run a test to see if the entire early Homo sample shows a trend over time (and it does), but it is clear from the data that the major difference is the shift in size from habilines to early humans, with each of these groups showing relatively little change over time.

The trend in A. boisei depends entirely on the earliest and latest fossils. The small size of the early Omo L338y-6 specimen is unsurprising compared to the even smaller KNM-WT 17000, so the idea that the A. boisei lineage should have changed over time is possibly expected. But Omo L338y-6 is not the smallest member of the later sample (KNM-ER 407 is smaller), so it does make a difference whether KNM-WT 17000 is excluded or not. Especially considering this is a robust probable male skull, its very small endocranial volume makes a large contrast with later A. boisei, a difference extended by many other anatomical details.

What about the late end of the sample? Here, the endocranial volume of KGA 10-525 appears very large, and is at the high end of the A. boisei range. But compared to earlier hominids, the volume is not surprisingly large. For example, the endocranial volume of AL 444-2 (A. afarensis) is estimated at around 550 mL (Holloway and Yuan 2004), and the volume of STW 505 (A. africanus) is certainly larger, perhaps over 600 mL (Hawks and Wolpoff 1999; Conroy et al. 1999). Although the body size of KGA 10-525 is not known, its molars are near the top end of the A. boisei sample, exceeded only by OH 5. This might suggest that the body size of the specimen was among the largest in the sample, and at the least we can guess that the individual was larger than the average for males.

So to address whether KGA 10-525 was surprisingly large, we have to look beyond its date and ask what the expected range of brain sizes within A. boisei would have been. Including KNM-WT 17000 at the small end, and KGA 10-525 at the large end, the standard deviation of the entire A. boisei sensu lato sample in endocranial volume is 39.3 mL. With an average volume of 480 mL, this yields a CV (coefficient of variation) of 8.2 percent.

By contrast, the H. habilis sensu lato sample, including KNM-ER 1470, has a standard deviation of 79.6 mL on an average of 634 mL, yielding a CV of 12.6 percent. So the A. boisei sample is a third less variable than the H. habilis sample.

Holloway (1980) gives CV values for recent humans, from the Danish data of Pakkenberg and Voight (1964), broken down by sex. The within-sex CV's for males and females were 8.2 percent and 8.3 percent, respectively. So the variation within the extant sample of A. boisei, including KNM-WT 17000, is about the same as within one sex in living humans. This is despite the fact that the A. boisei sample spans a million years of time and appears to have been substantially greater in body size dimorphism (as indicated by cranial robusticity and tooth sizes) compared to humans.

Tobias (1971) pools data from several earlier studies of endocranial volumes in hominoids, pooling sexes together. In his summary, the smallest degree of variation is within white-handed gibbons (Hylobates lar), where the CV of endocranial volume is 7.6 percent. Other hominoids are higher: chimpanzees at 9.7 percent, siamangs at 10.7 percent, orangutans at 10.9 percent, and a male-biased sample of gorillas at 13.1 percent. Except for the small and monomorphic gibbons, all these are higher than the estimate for A. boisei.

So the problem is not that KGA 10-525 is surprisingly large. Instead, the problem is that variation in A. boisei has likely been substantially undersampled. There should be many larger and smaller crania than have yet been found in the sample.

This is a problem for testing whether there is a significant trend within the A. boisei sample. In a sample with relatively low variation, the observation of a single large specimen at the recent end of the sample may be statistically surprising--the rarity of the large size is combined with the rarity of the recent date.

In a study of fossils, we cannot really know what the underlying variability of the extinct species was. For this reason, we are left with tests that use only the observed sample variability. The best of these are randomization tests, which randomize one or more elements of the sample to determine the likelihood that the sample would have the observed characteristics based on the data at hand. But randomization tests assume that the data themselves are sufficient to represent the variation in the underlying population. If there is good reason to think that the data are not representative, then the randomization tests may mislead about the chance that the data would be ordered in the observed way at random.

What if instead of randomly ordering the data to test its significance, instead we modeled the characteristics of the underlying population. For example, we could assume that the population had been a single species with a standard deviation similar to that observed in some living or fossil species--perhaps the observed standard deviation for earlier hominids, or for recent humans. The null hypothesis would be that this population was static in mean endocranial volume. With the computer's help, we can draw random variates from a normal distribution with the assumed standard deviation, assigning them randomly to the times observed for the real fossil sample. Then, we can perform whatever statistic we prefer upon the simulated sample, repeating the process some arbitrarily large number of times. The number of times that meet or exceed the trend observed in the fossil sample provide a p value for the null hypothesis.

What would the result of such a test be for the A. boisei sample? Good question. I'll tell you when I find out.

Why is this important?

The question is really whether the brain size increase in Homo was unique among the early hominids, or whether it may have been replicated in other species. In particular, if the brain size increase also happened in A. boisei in parallel with early Homo, that would be surprising. After all, A. boisei likely had a very different paleoecology than any member of Homo, one that was almost certainly less dependent on technology, less reliant on high-energy foods such as meat, and presenting less of a necessity for group coordination of activities. If brain size increase could occur in a significant way in A. boisei, it really raises questions about the pattern of selection on brain size in hominids.

What could explain an increase in A. boisei? One hypothesis would be energetics. The brain is a great energetic drain, because nervous tissue is very costly. For this reason, there is normally fairly strong selection in favor of smaller brains--because they are more energetically efficient. This selection for smaller brains is opposed by selection for brain functions of one kind or another, because a brain that is too small risks losing some function important for survival or reproduction.

A. boisei clearly differed from earlier hominids in its dietary adaptation, and diet determines the overall energy budget available for an organism. Suppose that the robust masticatory adaptation of A. boisei allowed the species to have a more dependable source of foods during periods of scarcity--because the range of fallback foods was extended into foods unavailable to other hominids, for example. If this were the case, then A. boisei may have had significantly less resource stress during periods of resource scarcity for other hominids, and may therefore have had less trouble meeting their energetic demands. This would mean that the selection against larger brains on the basis of their energetic disadvantages might well be weaker in a robust australopithecine. With other sources of selection on brain function the same--or even possibly increased due to a small reliance on rudimentary toolmaking or other mental adaptations--the brain would increase in size.

Some have used the apparent increase in brain size in A. boisei as an argument to address the importance of brain size expansion in later Homo. This is a point worth addressing, because it is a potentially misleading comparison. One way that it misleads is in the magnitude of change necessary to explain the apparent trends. In A. boisei, a straight regression through the earliest and latest observations indicates an increase in brain size of roughly 70 mL per million years. Of course, this regression like all others is most influenced by the smallest and largest values on the independent axis. Considering the probability that KGA 10-525 was actually larger than its instantaneous average, and that Omo L338y-6 was actually small, the actual amount of change in the species over time was likely much less than 70 mL per million years. A consideration of the data points excluding these extreme values yields a nonsignificant increase of only 21.5 mL per million years.

In contrast, the magnitude of the increase in endocranial volume in Middle Pleistocene humans is much larger. Over the past million years, humans have increased from an average of around 900 mL to the present average of around 1350 mL, for a rate of 450 mL per million years. This is at least fivefold and more probably twentifold higher than the rate in A. boisei, and does not consider the observation that the change was concentrated in the more recent Middle and Late Pleistocene. Moreover, this rate is indeed a difference between early and late average values rather than a regression including early and late extreme values. One might object that we should consider the rate of change relative to the current absolute size rather than the absolute change. From the perspective of selection and the function of brain tissue, this question is not easy to answer: it could go either way. But a strict consideration of relative brain increase as opposed to absolute brain increase still shows that recent humans increased at a rate probably seven to tenfold higher than in A. boisei. And the increase within the past 250,000 years--from approximately 1100 to 1350 mL--would indicate a much higher rate of change, at 1000 mL per million years.

So the observation of a slight trend toward higher brain size in A. boisei would not diminish the impressive degree of change in recent human evolution. Nor does it really lend to the idea that brain increases were widespread among fossil hominids and therefore unsurprising. In all likelihood there were other surprising changes, such as the increase from Australopithecus to Homo, and the increase from H. habilis to early humans. Each of these changes deserves a unique explanation, since the brain is not a character likely to increase in size at random or under the influence of genetic drift. And since the most recent increase in Pleistocene hominids occurred in every inhabited region of the world, it would require either gene flow between regions or several unique cases of simulaneous parallel evolution to explain.

Bottom line: is there anything to explain here in A. boisei? I don't really think so. The apparent trend is too likely to be generated by the outlying observations. Even if a trend existed in the species over time, it appears to have been pretty low in magnitude. This remains a case where the recovery of a single specimen with the right measurements and date would completely eliminate any statistically significant result.

References:

Conroy GC, Weber GW, Seidler H, Tobias PV. 1999. Endocranial capacity of early hominids. Science 283:9.

Elton S, Bishop LC, Wood B. 2001. Comparative context of Plio-Pleistocene hominin brain evolution. J Hum Evol 41:1--27.

Hawks J, Wolpoff MH. 1999. Endocranial capacity of early hominids. Science 283:9b.

Holloway RL. 1980. Within-species brain-body weight variability: A reexamination of the Danish data and other primate species. Am J Phys Anthropol 53:109--121.

Holloway RL, Yuan MS. 2004. Endocranial morphology of A. L. 444-2. In: Kimbel WH, Rak Y, Johanson DC, editors, The skull of Australopithecus afarensis. Oxford, UK: Oxford University Press. p 123--135.

Lee SH, Wolpoff MH. 2003. The pattern of evolution in Pleistocene human brain size. Paleobiology 29:186--196.

Pakkenberg H, Voigt J. 1964. Brain weight of the Danes: forensic material. Acta Anatomica 56:297--307.

Tobias PV. 1971. The brain in hominid evolution. Columbia: New York.

In his 2003 book, Lowly Origin, Jonathan Kingdon presents a model for the origins of hominid bipedality, along with many other possible insights concerning the evolution of both earlier apes and later hominids. The book is notable because of Kingdon's speciality: as a very talented zoologist and perhaps the foremost biogeographer of African mammals, he brings an eye toward the temporal and spatial context of the transition to bipedalism that is generally lacking in other models. The book is also notable because it is recent, and provides a present-day look at many venerable models of hominid origins that well characterizes their strengths and weaknesses with respect to the present pattern of evidence.

An example of his biogeographical knowledge coming into play is his hypothesis for the place that bipedalism may have originated. Many models talk about a hypothetical division between Central African and East African forests or a hypothetical mosaic forest-savanna woodland mix. Kingdon can talk about actual forests where this might have happened. He focuses on the coastal African forest, which stretches from Somalia to South Africa (116-119). His examinations of biogeography of microfauna have shown that this forest has been biologically separate from those of Central Africa for a very long time. Today, the coastal forest is depauperate of large and medium-sized endemic mammals, which Kingdon attributes to human activity during the past 40,000 years. In the past, this forest would have served as a core area for animals spreading periodically into river valleys and forest fragments further inland. It would also have presented a rather different climate regime from the West and Central African forests, with its highly seasonal monsoonal rainfall.

Filling the bill

Any model that attempts to explain hominid origins must provide an account of several distinct things:

1. How did early hominid populations become separated from early chimpanzee populations? That is to say, what accounts for the human-chimp divergence?
2. What decisive advantage was there in increasing the frequency or importance of bipedal locomotion?
3. What exactly was the ancestral pattern of locomotion?
4. Why did this ancestral pattern, whatever it was, lose its advantages when compared to bipedality?

To question number 1, Kingdon gives basically the same biogeographical answer as Coppens' East Side Story and many others: namely, that progressive aridification of East Africa led to a separation of East and West African ancestral hominoids. His details about the nature of the East African forest are very welcome and interesting, but do not change the basic picture. Kingdon places the timing of this event in several cycles of aridity beginning at 10.5 million years ago, through recurrent drying at around 7.8 million years ago and 6.2 million years ago (119). These dates do approximately correspond with the time interval preceding the fossil remains of the earliest hominids, which are now some 6 million years old.

To the second question, about the advantage of bipedalism, Kingdon provides an answer based on Clifford Jolly's (1970) seed eaters hypothesis. In this model, and upright posture for the upper body is advantageous for use in foraging for small items, in particular seeds from grasses. Like Jolly, Kingdon envisions a squatting, ground-based ape, which he calls the ground ape. He describes the effects of a small item feeding strategy as follows:

One way of asking how apes might have responded to these limitations is to look at the feeding strategies of living species. For example, when contemporary chimps are under duress from a poor fruit season, they break up into smaller foraging units that scour the environment more thoroughly while trying to maintain their frugivorous dietary preferences for as long as possible. By contrast, the more terrestrial gorillas respond to the same pressure by maintaining their groupings but diversifying and enlarging the range of their foods to include previously ignored and less digestible plants. Another variant, better suited to eastern forests, would have been to diversify (by including more animal and underground foods) but also to spend more time and effort foraging for smaller (but still nutritionally rewarding) items. As observed in contemporary situations, these are stopgap routines for gorillas and chimpanzees. However, I am proposing that similar strategies could develop or be transposed into a sustained and systematic way of using a spatially restricted environment. (122-123)

When Jolly originated the small object feeding model, he focused on the analogy between geladas and savanna baboons as a way of understanding the effects of this dietary change. Kingdon focuses more closely on the range of plant species that may be exploited by such a dietary shift, the ability of ancient groups to exploit the same geographic range more intensively, and the probable ecological diversity of plant species in the East African forest. He notes that chimpanzee groups across Africa appear to use a similar number of fruiting plant species, adjusting their home range in response to habitat richness. This results in a great disparity in chimpanzee foraging ranges (from as little as five square kilometers to as much as 400 square kilometers). Kingdon suggests that a more intensive foraging strategy based on the wider ecological diversity of East African forests may have increased the carrying capacity of these forests for the ground apes, with consequent alterations in their social behavior and ecology. He supports this ecological model with an analysis of the species richness of human-edible plants in this eastern forest (123). His major case is based on the increased availability of ground or near-ground foods in the eastern forest, including both animal and plant resources, compared with the small ratio of time that forced chimpanzees appeared to spend foraging near the ground as opposed to foraging canopy fruits

Perhaps the most important change, in answer to question 4 above, is a change in daily foraging range. As Kingdon notes, "Quadrupedalism would never have been abandoned if substantial distances had to be covered, especially if such journeys involved exposure to predators" (125). Easy terrestrial movement and escape from predation in apes requires the rapid movement of quadrupedal locomotion. It biped faces substantial disadvantages in these respects. This means that a greater reliance on bipedal locomotion would has required both a small home range and easy access to trees. This idea is a 180 degree shift from the Darwinian model of bipedal origins, in which upright posture was a reflection of the challenges of a poor habitat and the need to forage over long distances. Here, it is safe "secure and a rich environment" that is essential to the origin of bipedalism. In Kingdon's view, living apes naturally pursue a number of hand manipulation skills, social interactions, gestural communication, and carrying objects that require them to "squat, lie down, stand on two legs, or become three-legged" (125). For all of these behaviors, bipedal locomotion might well be naturally advantageous. But chimpanzees and gorillas cannot abandon quadrupedal locomotion and its speed advantages because of their large foraging ranges and susceptibility to predation. The commitment to quadrupedalism thereby impedes the further development of manual abilities that apes already have.

This idea provides a slightly different answer from Jolly might have given concerning why geladas are not more hominid-like than they are. Although the foraging style of manipulating small hard seeds and other objects might have been similar between early hominids and geladas, the habitat is very different. Geladas must retains an effective adaptation to quadrupedalism because they do not limit their foraging to areas where trees are readily accessible. Nor do they already show the range of manipulative behaviors shared by apes, which provided further incentives to bipedalism in early hominids.

The thrust from squatting

The squat-feeding model encompasses several untested predictions, which might well provide fertile ground for research. First, this pattern of adaptation should direct attention to the anatomy of the back. In particular, to conserve energy and maximize the use of a single foraging location, the spine should be well adapted to a bright posture, flexible in side to side movements, and capable of providing a stable platform for a wide range of movement for the arms. This may help to answer the question of why early hominids had relatively long spines, and especially in contrast with very short lumbar spines in other living hominoids. It also allows the side-to-side twisting motion of the pelvis during bipedal gait to be examined as an exaptation based on an earlier ability to rotate the upper trunk against a stationary pelvis. Normal arm-swinging upright walking depends on this flexibility of the lower spine, which would appear to be absent from living chimpanzees and gorillas, in which the flat iliac blades and the lower rib cage are strongly connected and relatively inflexible. Kingdon describes the compact, inflexible trunks of living apes (127) and their disadvantages for upright walking, but he does not explore why this configuration in apes would be advantageous for the locomotor behaviors of these apes, such as climbing or knuckle-walking. This difference from hominids is worth exploring, particularly in considering the effectiveness of early hominids as climbers.

The model also places a different spin on the usual anatomical description of the changes involved in bipedalism. Generally, the shortening and broadening of the iliac blades are seen as enabling a shift in muscular action during hip extension, recruiting the gluteus maximus as an extensor of the hip instead of an abductor. Kingdon explains the shortening of the iliac blades as a way of disentangling their action from the motion of the lower trunk, creating two separate functional units. In this way, he also explains the lengthening of the lumbar spine as part of the same anatomical change. This is potentially important because the length of the lumbar spine in the common ancestor of hominids and chimpanzees is not known. If hominids descended from an ancestor with the chimpanzee-like spine, a mechanism for the expansion in length of the lumbar spine is both necessary and welcome.

One of the advantages of bipedal locomotion often cited in explanations of hominid origins is the ability to see distances over tall grass while scanning for predators. Kingdon places a different twist on this also, by suggesting that this scanning behavior was present prior to the evolution of obligate bipedalism, as the ground apes would scan for predators from a squatting position. In this way, the apes habitually made their spines as vertically erect as possible at frequent intervals, and simultaneously required effective side to side head movement. This kind of behavior may have underlain the anterior placement of the foramen magnum and the reconfiguration of the head-spine articulation. This hypothesis would especially be interesting if it were shown that the anterior placement of the foramen magnum significantly predated the origin of the pelvic specializations for bipedalism. This kind of evidence might already be present in Sahelanthropus, Orrorin, or Ardipithecus. Especially in Sahelanthropus, where Brunet and colleagues (2002) have argued for an anterior foramen magnum, and in the Aramis occiput, where the foramen magnum also appears to be relatively anterior. Pelvic evidence is not yet available from any early hominid, and although the Orrorin femora are consistent with the weight-transmission characteristics of later hominids, it is not clear that this anatomical element is necessarily reflective of an entire pelvic anatomical complex.

One might argue that every hypothesis to explain the origin of bipedalism is in some sense an umbrella hypothesis (Langdon 1997), and this is no exception. While the fundamental change hypothesized by the model is a change in foraging strategies, this change is proposed have several effects on other elements of early hominid behavior.

The first of these involves the dynamics of hominid groups. Kingdon speculates that terrestrial life would have involved new adaptations to resist a greater diversity of predators and competitors. This adaptation would likely have involved group coordination with intimidation displays. In particular, a restriction to relatively small home ranges would of reduced the possibility of simply moving on as a response to competition or predation. Climbing would have remained very important in predator avoidance, but it arguably would not be enough to cope with the eastern African ecology.

Speciation among the early hominids

Another consequence adduced by Kingdon is on the pattern of speciation of subsequent hominid lineages after the hominid-chimpanzee divergence. Kingdon describes many of the land areas bordering on the East African coastal forest, along with the prospects for ancestral hominids occupying and spreading among these different areas. He raises an interesting point about the Zambezi basin, which is largely open grassland with extensive floodplains and gallery forests and would therefore have been ideal hominid habitat despite the present lack of hominid fossils from the area.

As Kingdon describes each African region, he makes four basic points. First, the linear movement of ground apes along the coast and into the upland regions would have placed hominid populations at such distance from each other to radically restrict gene flow between them. Second, each of the areas, ranging from the Ethiopian highlands to the Zambesi basin would have presented unique ecological circumstances that would have demanded local adaptations on the part of the early ground apes. And third, the likely habitat of the ground apes extended along river courses. This means that the apes were likely not separated by the river drainages themselves, especially since many of them are highly seasonal, but instead they were separated by the interim habitats that were highly risky and resource-poor for a woodland-dependant ape. Last, the home ranges of the ground apes were probably small, again reducing the possibility of long-range dispersal and contact among populations.

I repeated the term "ground ape" repeatedly in the previous paragraph in reflection of Kingdon's other major assumption. He promotes the ground ape as a genuine stage in the evolution of the hominids. In other words, these apes once differentiated from chimpanzees were themselves highly successful occupants of the East African forest, and could themselves spread into adjacent habitats. All this occurred before the advent of of bipedalism as reflected in later hominids. This would imply that a substantial diversity of ground apes may have once existed, on the hominid lineage, but not themselves obligate bipeds. Kingdon suggests that known fossil samples like Orrorin or Ardipithecus might in fact represent a ground ape in this sense rather than bipedal hominids.

I am unconvinced by the idea that the squatting ground ape lived for a long period of time before evolving the adaptations to effective bipedality. Indeed, Kingdon's argument about the advantages of bipedalism would seem to suggest that it would emerge quickly if the opposing need for quadrupedal locomotion decreased. The idea that the ground ape stage lasted for a long time ignores the likelihood of competition from more effectively arboreal forms.

The biogeographic separation of hominid ancestors from chimpanzee ancestors (and gorilla ancestors) creates a set of interesting problems that Kingdon doesn't address. For example, if the apes on both sides of the East African arid strip were initially the same, did this original ape form survive for some time alongside the new ground apes? Or was that form itself a ground ape (as speculated below). Did this ancestral species survive alongside its bipedal descendants for some period of time? If Kingdon's idea about widespread diversification and long survival of the ground apes were true, then these apes must have coexisted for some long time with their bipedal descendants, especially if the ground apes had significant local adaptations to different African regions.

While Kingdon does support his argument that the early ground apes would have differentiated into different species with several assumptions, I found this unconvincing. Consider that chimpanzees are spread across over three thousand miles of West and Central Africa with clear evidence of recurrent gene flow among different subspecies over the past million years or more. Lowland gorillas also have an impressive geographic range, and orangutans today comprise two long-lasting geographic subspecies, which in the past must have extended to a greater diversity on the Asian mainland as well as across the Sunda shelf. The phylogenetic pattern represented by today's great apes indicates widespread species with highly conservative ecological adaptations. This allows subspecies to remain ecologically similar for long periods of time, and enables the exchange of genes long after the initial establishment of geographically distant (or periodically isolated) populations.

Kingdon does not consider this pattern, but his argument would indicate that the ground apes (or early hominids) diverged from the phylogenetic tendencies of other ape species because of their restricted home ranges and more intensive ecological exploitation of local environments. This hinges on the idea that bipedality really doesn't increase mobility, but instead radically decreases it.

But this argument fails to recognize the energetic consequences of bipedalism after it originates. It may be true that the initial transition to bipedalism would not be possible without the means of abandoning the dependence on quadrupedal movement in foraging and flight. It may also be true that obligate bipeds continued to be at a disadvantage compared to quadrupeds in predator avoidance and daily range. But the movement of bipeds over long distances would if anything have been less costly than that of a quadruped of the same size. And the social correlates of bipedality that Kingdon notes would seem likely to increase dispersal rather than decrease it. That is to say, despite a smaller home range, more cohesive groups with potentially larger group sizes present a higher chance of significant disparities in resource access among groups, a greater variance in group sizes, increased challenges for individuals integrating into new groups, and greater incentives to colonize and disperse over long distances. Bipeds are well equipped to move along linear habitats like gallery forests, and might have done so with maximum energetic efficiency in response to resource challenges or seasonal scarcity. An increased tolerance for higher population densities would have enabled an effective migration strategy in regions where seasonal resource shortfalls in one area may have been supplemented by movement to other areas with enough to go around.

This cuts to the nature of what it is to be a biped. Once the bipedal strategy arose, did it enable greater mobility or not? Were hominid groups highly territorial, and highly sedentary, or were they instead highly mobile? Did hominids tolerate local aggregations of multiple groups, or were they committed instead to intergroup conflict? This is where a chimpanzee model potentially misleads, since chimpanzees are both mobile and territorial, intolerant of contact with neighbors and capable of long-distance dispersal for maturing females. How would bipedalism change a chimpanzee's behaviors? An unanswered question.

Unanswered questions

An unanswered question is to what extent the focus on ground-accessible foods would have precluded the use of canopy foods. As Kingdon notes, canopy fruits are the major food source for chimpanzees today. Presumably, a greater adaptation to terrestrial life including bipedal locomotion would have greatly restricted the ability of early hominids to climb into the forest canopy and exploit fruiting trees. It seems possible that competition from other primates, such as cercopithecoid monkeys, might have precluded the effective dependence on a canopy resources anyway. But this line of inquiry needs to be developed further.

Another unanswered question involves the body proportions of early hominids. Australopithecines were exceptionally short compared to living humans. And there legs were hardly longer than similar-sized apes. These legs were very inefficient for bipedal movement compared to the long legs of subsequent hominids. But one possibility is that australopithecine legs may have been effectively adapted to a squatting posture. As far as I know, this hypothesis remains to be tested. Certainly if Kingdon is right about the small foraging ranges
of early hominids, the energetic disadvantages of short legs may have been relatively minor, because hominids would never have walked very far anyway. In this respect, even the home ranges of chimpanzees would be a poor model for the relatively small home ranges of early hominids. While anthropologists have tended to contrast australopithecines with early humans, who were believed to have had larger home ranges on the scale of those occupied by living hunter gatherers, it remains possible that australopithecine home ranges were smaller even than has usually been assumed.

And of course the biggest unanswered question appeared in the form of a key fossil shortly after the book must have been finished. What about Sahelanthropus? If Sahelanthropus was in fact on the hominid lineage, then it would seem to reject the model of differentiation proposed by Kingdon--Chad is a long way from the East African coastal forest. Conversely, if it is not on the hominid lineage, its importance to the model depends on what it is. If it is ancestral to hominids or to chimpanzees or gorillas, then it potentially informs us as to the anatomy of the common ancestor to these species. If so, that ancestor may have been substantially more ground ape-like than even Kingdon might have expected, at least if Brunet and colleagues (2002) are right about the foramen magnum placement and its implications for vertical posture. One might even envisage the hypothesis that chimpanzees and gorillas themselves are substantially derived from the common ancestor because they colonized the West and Central African equatorial forests long after the common ancestor lived (although presumably before the separation of chimpanzees and bonobos). This is a lot of mileage out of one fossil sample, but the absence of a fossil record for either chimpanzees or gorillas invites speculation.

References:

Brunet M, Guy F, Pilbeam D, Mackaye HT, Likius A, Ahounta D, Beauvillain A, Blondel C, Bocherens H, Boisserie JR, De Bonis L, Coppens Y, Dejax J, Denys C, Duringer P, Eisenmann V, Fanone G, Fronty P, Geraads D, Lehmann T, Lihoreau F, Louchart A, Mahamat A, Merceron G, Mouchelin G, Otero O, Campomanes PP, Ponce de Leon M, Rage JC, Sapanet M, Schuster M, Sudre J, Tassy P, Valentin X, Vignaud P, Viriot L, Zazzo A, Zollikofer C. 2002. A new hominid from the Upper Miocene of Chad, Central Africa. Nature 418:145Ð151.

Kingdon J. 2003. Lowly origin: Where, when, and why our ancestors first stood up. Princeton, NJ: Princeton University Press.

Langdon JH. 1997. Umbrella hypotheses and parsimony in human evolution: A critique of the Aquatic Ape Hypothesis. J Hum Evol 33:479Ð494.

James R. Flynn is a social scientist at the University of Otago, New Zealand. Beginning in 1981, Flynn performed a series of statistical analyses on the results of IQ tests in Western populations. The analyses showed that IQ scores in every population measured are systematically rising over time, with each succeeding generation apparently smarter than its predecessor. These IQ gains have been dubbed the "Flynn effect," and the causes and patterns underlying these changes are still obscure. Flynn recounts the story of his findings in his article "Searching for justice: the discovery of IQ gains over time," in the January 1999 issue of American Psychologist, as well as discussing the current state of research into IQ changes and the moral and sociological corollaries of the research.

The initial finding of rising IQ came from looking at the pattern of correlations between successive versions of IQ tests. When publishers came up with revised versions of tests, they would apply both the new and old test to a set of the same subjects. If the subjects scored similarly on both versions of the test, it would demonstrate that the new test was measuring the same skills as the old test. But Flynn noticed something else about these results: the subjects who took both versions of the test would average a significantly higher score on the older version. Since the older version's scores were standardized at the time it was written, Flynn noted that "the only possible explanation was that representative samples of White Americans were setting higher standards of test performance over time" (5). In this first analysis, the IQ gain from 1947 to 1972 was 8 points. In a broader sample of tests, "the rate of gain was about 0.30 IQ points per year, roughly uniform over time and similar for all ages" (6, citing Flynn 1984).

In light of these results, Flynn gathered data on IQ surveys in as many nations as had routine military induction testing or other large-scale testing organizations (6). The startling result was that IQ has been increasing in every one of these countries, and that the increases were especially noted in tests that were thought to be less susceptible to biases from educational or cultural factors. The longest-term sample was available from Britain, where it became clear that the fifth percentile among persons born in 1967 was equivalent to the ninetieth percentile of those born in 1877 (Raven et al. 1998).

What should we make of this phenomenon? According to Flynn (7):

This deals a stunning blow to our confidence in the ability of IQ tests to compare groups for intelligence, at least when those groups are separated by cultural distance. Can anyone take seriously the notion that the generation born in 1937 was that much more intelligent than the generation born in 1907, to say nothing of the generation born in 1877? It also deals a blow to the Spearman-Jensen theory of intelligence. That theory is based in g, the general intelligence factor derived from the tendency of the same people to excel on a wide range of IQ tests.

Flynn relies on common sense to justify this intuition, but to the extent that the results would seem to indicate very surprising conclusions, his common sense appears to be sound. As he notes, it seems unlikely that high proportions of earlier generations would have lacked the intelligence to understand the rules of popular sports. And as he notes (7), "[achievement gains] fall away the closer we come to the content of school-taught subjects" such as "arithmetic, information, and vocabulary."

He also gives a quick rundown of the reasons suggested to explain the IQ rise over time, along with reasons why they cannot explain the entire problem. His passage on the effect of better nutrition is well worth reading. Each section is a reminder of the nature of the problem: first, can these reasons explain IQ gains that were progressive, gradual, and constant, and second, are we really to believe that earlier generations actually had intelligence as low as their scores compared to today's scores would indicate?

The social justice element of the article comes from the consideration of how apparent IQ gains affect the interpretation of race differences in IQ test performance. One section is spent considering the ways that group achievement in real terms may not represent the expectations from their IQ scores compared to other groups. Flynn focuses on the cultural and educational differences among groups as a way to explain differences in outcome that are not predicted by IQ scores.

In a second section, Flynn lays out the issues surrounding the interpretation of race differences in IQ as applied to American Blacks and Whites (his terminology). In this, he gives a thoughtful presentation of the Jensen position. This contains a very clear presentation of the concept of regression that is worth quoting (13):

The key to what follows is the concept of correlations as measures of regression toward the mean. To provide a simple example: Imagine that the correlation between height and between-family environment was perfect, or 1.00. The significance of that would be this: If we found a group one standard deviation below the mean for height, and environmental factors were solely responsible for their height deficit, then they should be one standard deviation below average in terms of environment. Now imagine the correlation is less than perfect, perhaps only .35. In that case, it would take several standard deviations of environmental deprivation to account for a one standard deviation height deficit. A bit of arithmetic shows it would take 2.86 standard deviations, because 2.86 times .35 equals one standard deviation. In summary, the correlation determines precisely how many standard deviations of environmental deficit it takes to account for a one standard deviation height deficit, or to be technical, it determines how far toward the mean the below-average group will regress as each standard deviation of environmental deficit is eliminated: clearly only 35% of the way.

As Flynn notes, Jensen's (e.g. 1972) case for Black-White IQ differences rested on the observation that between-family environmental differences had a correlation of .35 with IQ within Whites. According the the example above, it would require a deficit of 2.86 standard deviations of environmental conditions in Blacks compared to Whites in order to explain the IQ difference. According to a normal distribution, this would imply that "the average environment of Black Americans would have to be inferior to that enjoyed by 99.79% of White Americans" (13). Jensen argues that such a difference is unlikely, but in particular examines the idea that such an environmental difference might exist by discussing what its likely effects would be. In his view, a factor like racism might account for IQ differences by affecting self-image, confidence, and other social factors. But as Flynn summarizes his argument, "Who could argue that these same factors do not vary significantly within the Black population? ... If these factors both are potent and vary among Blacks, why do they explain so little IQ variance within the Black population?"

Flynn discusses Lewontin (1976) in particular as someone who argued for an environmental explanation by means of a thought experiment. Certainly there is no theoretical difficulty in imagining a nongenetic difference that would cause differences between groups without causing significant within-group differences. But one must imagine that the environmental difference was uniform within each group, which is arguably not true of any real-life human environmental variable. In Flynn's view, Lewontin's example merely begs the question of the real differences between races, since Lewontin provided no real-world example that would credibly avoid Jensen's objections.

Flynn describes his own attempts to address this issue. The major piece of evidence he drew upon (Flynn 1980) involved the IQ scores of children of the American occupation of Germany after World War II. Both Black and White American soldiers fathered children with German women, and the IQ scores of both groups of children were almost identical. Flynn argued that direct evidence of this kind, reflecting what actually occurs when different races are subject to qualitatively similar environments, is more important than the kind of indirect evidence that comes from attempting to correct samples for socioeconomic status or other environmental variables.

In addition to this kind of direct evidence, Flynn argues here that the observation of IQ test gains over time further reduces the relevance of the indirect evidence of environmental differences. For one, the gain of IQ from one generation to the next must certainly be almost all, if not entirely, due to environmental change. Flynn presents this as a real-world example that fits Lewontin's model, above, where within-group differences are mostly genetic, while between-group differences are mostly environmental in origin. (This also plays into a continuing current theme in Flynn's research examining how IQ can continue to increase while remaining fairly strongly heritable. This itself appears paradoxical, since continued environmental gains would normally be expected to reduce the heritability by decreasing potential environmental variance.) Second, the magnitude of the IQ gains is so large, that the Black-White average IQ difference seems comparatively minor (15):

As for the environmental gap one must posit to explain the Black-White IQ gap, IQ gains over time pull this out of the stratosphere and down to earth. It appears that Blacks have enjoyed a slightly higher rate of gain on Wechsler-type tests than Whites (Herrnstein and Murray 1994, pp. 277, 289). This implies that since 1945, Blacks have gained at an average rate of over 0.30 points per year and have gained a total of 16 points over 50 years. Therefore, the Blacks of 1995 should have matched the mean IQ of the Whites of 1945. Therefore, an environmental explanation of the racial IQ gap need only posit this: that the average environment for Blacks in 1995 matches the quality of the average environment for Whites in 1945. I do not find that implausible.

Of course, this still leaves unexplained just why the IQ gains have occurred and whether they actually reflect differences in some mental properties beyond the process of psychometry. So as an account of race differences, it is not entirely satisfactory. But it does show quite clearly that the kind of environmental differences that would be sufficient to explain racial differences in IQ as measured today are very much within the range of environmental changes that must have occurred in a historical context. For that reason, we have every reason to think that the environmental differences between groups today might be very large, and sufficient to explain observed differences in IQ scores. Or as Flynn puts it (16): "The appropriate rejection of Black genetic inferiority is this: Nothing at present coerces rational belief."

The penultimate section of Flynn's paper concerns the relationship of IQ with class membership, the thesis of Herrnstein and Murray's The Bell Curve. Here, Flynn does something very interesting (this section is derived from a longer 1996 paper in the Journal of Biosocial Science). Most critiques of The Bell Curve have focused on the race differences aspect of the book. But Flynn takes a greater interest in the aspect of the book that focuses on the idea of a natural meritocracy, for which IQ scores are assumed to be a correlate (16):

[Race differences are] a distraction from the real challenge The Bell Curve poses. The humane-egalitarian concept of social justice includes more than compensating people who suffer because of their group membership. It gives high priority to certain ideals, such as reducing environmental inequality and social privilege to tolerable levels. Herrnstein and Murray (1994) went beyond race to level the most devastating possible critique of those ideals, namely, that they self-destruct in practice. I refer to the meritocracy thesis, which runs as follows. The closer we come to environmental equality, the more all talent differences become caused by genetic differences. The more we eliminate privilege, the more we have total social mobility, and good genes for talent rise to the top and bad genes sink to the bottom. The tendency to marry those of similar IQ produces mating couples whose social status correlates with genetic quality. The result is an elite class whose children replicate their parents' high status, because of luck in the genetic lottery, and a large immiserated underclass whose children, handicapped by their bad genes, cannot escape low status.

Flynn presents an argument against this "meritocracy thesis" that claims the thesis is psychologically incoherent. It is not enough to show that an IQ elite is not already emerging, for although the evidence clearly shows that class differences in IQ are not increasing, that does little to assuage the moral difficulties that emerge from the concept of a true meritocracy. For there can be little argument that a reduction in environmental differences between people is a goal of "enlightened" social policy; it is, after all, the very meaning of "equality of opportunity." If the emergence of strong and permanent class differences based on genetic differences were a natural consequence of true equality of opportunity, one might well question the social value of such policies.

But Flynn argues that the meritocracy thesis is internally incoherent. It proposes that if social and environmental inequalities were eliminated, a strong ordering of people by class according to their innate talents would result. Because of equal environments, variation in talents would be largely genetic, and would therefore be increasingly resistant to change. But consider that social stratification occurs precisely because of the striving of individuals for greater status, wealth, prestige, and other indices of social inequality. Flynn essentially argues that Herrnstein and Murray (1984) unjustifiably project the current value of materialism and elitism into a hypothetical future, one which is predicated on the absence of the current level of materialism and elitism. In other words, the meritocratic future depends on strong notions of social competition based on wealth (or other markers of status), but the establishment of such a future depends on eliminating most differences in wealth and status. Or more directly (18):

The case against meritocracy can also be put sociologically: (a) Allocating rewards irrespective of merit is a prerequisite for meritocracy, otherwise environments cannot be equalized; (b) allocating rewards according to merit is a prerequisite for meritocracy, otherwise people cannot be stratified by wealth and status; (c) therefore, a class-stratified meritocracy is impossible.

Thus, the idea of an "immiserated underclass" seems inconsisent with the assertion that environments are qualitatively equal. But "if all have decent work, housing, education, health care, security in old age, what remains is not essential for happiness. Many people of talent may want more than the not-unattractive minimum, but ho many will care about shaking the last dollar out of the money tree?" (18). Flynn concludes (18):

Analysis of the meritocracy thesis provides not only a rebuttal but also a better understanding of the dynamics of humane-egalitarian ideals. The truth is that we cannot push equality much beyond our capacity to humanize. Every significant step toward equality must be accompanied by an evolution of values unfriendly to success as defined by the present class structure. Humane-egalitarian ideals possess a great glory: a self-correcting mechanism that avoids meritocratic excess. Whatever dark spirits lurk in the depths of equality, meritocracy is not among them.

I find this part the most intriguing, because it invites some expectations about ancient human societies, and the probable correlates of intelligence. Clearly, intelligence (broadly construed) in humans has both genetic and environmental components. Likewise, other traits including status (wealth is less relevant in a Pleistocene context) and of course fitness have both genetic and environmental components. Each of these traits was likely correlated to some extent with the others, and to the extent that each trait was correlated with fitness and was heritable, it would be under selection.

In this context, humans had every reason to increase their fitness through systematic alteration of the environmental component of these traits. Some aspects of the environment would be largely outside their control. For example, maximizing nutrition must have been a constant struggle for all people largely at the mercy of local ecological conditions. Other aspects could have emerged from interesting patterns of social interaction. For example, practical intelligence (as applied to problems of survival and reproduction) must have been greatly influenced by other people, through teaching, observation, learning feedbacks, storytelling, and other opportunities. It seems plausible that the environmental component of this kind of intelligence would have been higher in Pleistocene societies than today. One reason is the likely diversity of social contexts in small groups with high mortality rates (such as the increased chance of absence of one or both parents).

This kind of interaction among variables creates a behavioral context in which not only the brain functions underlying intelligence-related skills would have been under selection, but also those functions related to enabling those functions to their maximum under the existing environmental regime. This latter selection would be highly kin-mediated, as the inclusive fitness of individuals depended partly on the intelligence of their relatives. For that matter, the direct fitness of individuals would depend on the realized intelligence of members of their groups in the long-term struggle for survival and differential reproduction. Consider:

1. These processes predict that group effects in human evolution might have been largely intelligence-mediated. Individual survival depends in part on the hunting effectiveness of group members, on their ability to maintain social ties with kin in neighboring groups, if they remember or not important information about ecological or climatic variability, etc. So it is in every individual's best interest to contribute materially to the education (meaning environmental maximization of operational intelligence) of other members of his or her group, related or not.
2. Any genetic advantages in intelligence mean little without substantial environmental equality within the population at large. This is because environmental differences in intelligence might easily outweigh any genetic advantage.
3. It goes without saying that people should have competed to the greatest extent possible for those material (or behavioral) circumstances that are associated with maximal environmental benefits for fitness. But if intelligence was correlated with fitness, then those circumstances most favorable for the development of intelligence should also have been subject to strong competition. These might include:
   1. preserving the lives of elders or others with valuable information
   2. recruiting new group members with certain properties conducive to greater group learning, such as good storytellers
   3. developing strong cultural justifications for the transmission of certain kinds of knowledge
   4. exercising mate choice based on behaviors related to intelligence

   and certainly others.

These ideas are suggestive. People were not merely involved in a struggle for survival and reproduction, in which intelligence may have been a factor. They were simultaneously locked in a meta-struggle, in which the determinants of intelligence were themselves judged among people and their social standing and other characteristics became dependent on them because of their value for the group, present and future kin, and their risk observed for neighboring peoples. These conditions were only genetic to a minimal extent. For the most part, this struggle took place within populations based on the fundamentally environmental variation that was always present and could not be eliminated (because it would always have been maintained by population pressure if nothing else). So the natural selection underlying the evolution of the brain was itself a side effect of a very powerful social structure with behaviors devoted to detecting intelligence and promoting it for basically selfish reasons.

References:

Flynn JR. 1984. The mean IQ of Americans: massive gains from 1932 to 1978. Psych Bull 95:29-51.

Flynn JR. 1996. Group differences: is the good society impossible? J Biosoc Sci 28:573-585.

Flynn JR. 1999. Searching for justice: the discovery of IQ gains over time. Am Psych 54:5-29.

Jensen AR. 1972. Genetics and education. New York: Harper and Row.