The "dark matter" of modern human origins

I'm just looking through the January/February 2008 Evolutionary Anthropology, which is all about modern human origins in Africa. The special issue resulted from a conference at Stony Brook, along with a few additions to round out the topic.

I'll have some things to say about these articles, but one thing struck me. I'll describe the problem:

Dan Lieberman's paper, "Speculations about the selective basis for modern human cranial form," discusses five categories of functional requirements that might have been involved in the evolution of the "modern" human cranial anatomy. Each of these imposes distinctive requirements on the form of the head -- not all of which are fully understood -- but all of which changed in ways that parallel the basic changes in cranial form of the Late Pleistocene.

But Tim Weaver and Charles Roseman's paper, "New developments in the genetic evidence for modern human origins," claims that the modern human cranial anatomy originated by genetic drift, without any substantial selection:

Evolutionary quantitative genetic analyses, in fact, show that Neandertal and modern human cranial differences can be explained by genetic drift, making it unlikely, at least for the cranium, that modern human anatomical features were spread by natural selection rather than a range expansion out of Africa. An important point is that these analyses do not simply compare the magnitude of the morphological differences between Neandertals and modern humans; they are multivariate tests of how the patterns of covariation across different cranial measurements compare to those expected for divergence by genetic drift. Natural selective hypotheses designed to account for Neandertal and modern human cranial differences would also need to show multivariate consistency with the observed patterns of variation. While it may be possible to imagine natural selective scenarios that mimic genetic drift for a single measurement, such as fluctuating directional natural selection, the scenarios become much less plausible for multivariate patterns of variation (Weaver and Roseman 2008:78).

Both these papers cannot be correct. A full text search of Lieberman's paper does not find the words "drift" or "random," and "neutral" only appears as part of "neutral horizontal axis." Yet Weaver and Roseman cite the neutrality of cranial form as the main evidence against Eswaran's model of an adaptive dispersal of cranial form. According to them, all of Lieberman's "speculations" must be wrong.

I thought maybe I could get some insight into this dilemma by reading Günter Bräuer's paper, "The origin of modern anatomy: by speciation or intraspecific evolution." That title sounds fairly clear -- if we're talking about a speciation of modern humans to explain their anatomy, that sounds like the kind of rapid change that ought to indicate selection of some kind.

Bräuer shows some skepticism toward Lieberman's ideas about cranial evolution:

In my view, Lieberman, McBratney, and Krovitz's interpretation that anatomical modernization can be boiled down to just a few autapomorphies or genetic changes will be difficult to accommodate within the current fossil evidence (Bräuer 2008:27-28).

OK, but does this disagreement mean that Bräuer is likewise skeptical of adaptive hypotheses to explain modern cranial form? Again, a full text search fails to find the words, "drift," "neutral," or "random." But neither does it find the word "selection." Bräuer is concerned with describing the pattern of evolution of the modern human cranial form, but is entirely noncommittal on the question of why it evolved. That would seem to be problematic in itself: wouldn't we expect a different pattern of evolution if natural selection caused the changes, than if genetic drift caused them? Wouldn't the two causes make different predictions about the role of speciation in the process?

I'll have more to write about Bräuer's interesting paper, but on this issue, I think that is all I can extract from it. Osbjorn Pearson's paper, "Statistical and biological definitions of 'anatomically modern' humans," has more to say on the issue. Pearson cites the work that suggests modern human cranial form evolved under random genetic drift, saying:

Ideally, one would like to partition morphological distance into differences due to genetic drift, adaptation, and environmental interactions with ontogeny. Recently, several promising studies have shed light on these issues, including the amount of morphological diversity in recent humans that likely reflects genetic drift and the effects of the toughness of foods on the cranial morphology and occlusion of nonhuman primates, retrognathic mammals (for example, hyraxes), and humans from different parts of the world. Nevertheless, much remains to be done before these relationships become completely clear (Pearson 2008:40-41).

He later suggests (p. 44) that "rapid morphological change due to drift during population bottlenecks" may be involved in the evolution of modern cranial form. On the other hand, Pearson also suggests that "selection for new, advantageous traits or genes, or some combination of the two [selection and drift]" may have occurred. That would seem fairly noncommittal.

However, Pearson's description of the series of events -- a stepwise, sequential series of anatomical changes ultimately in a worldwide context up to and including the Holocene -- seems pretty unlikely to result from genetic drift alone. Indeed, Pearson writes,

In common with many other parts of the world, [African] crania that have dimensions or suites of morphological traits that make them statistically indistinguishable from the living populations appear only during the Holocene (Pearson 2008:45).

If the evolution of modern cranial form is a process that continued into the Holocene, it is quite impossible to have been caused by drift alone, since the effective population sizes of human populations were too large, and drift could hardly have caused a "nearly universal pattern of gracilization" (ibid.). So Pearson's paper certainly heightens the contrast between the adaptive and drift scenarios. If the events are as Pearson describes them, the "genetic drift alone" hypothesis must be false.

Philip Rightmire's paper is about earlier events, and Chris Stringer and Nick Barton's paper is a conference review. That leaves only Ian Tattersall and Jeff Schwartz's paper, "The morphological distinctiveness of Homo sapiens and its recognition in the fossil record: clarifying the problem," to clarify the problem.

Tattersall and Schwartz direct their attention to the kinds of features that are suitable for identifying a species from the fossil record -- uniquely derived features, or "autapomorphies." In their view, species must be accurately diagnosed from sets of specimens ("alpha taxonomy") before any kind of evolutionary hypotheses can be tested.

Because of this, they don't talk very much about the kinds of evolutionary forces that might cause the patterns they see. The paper includes only one reference to "random" and "adaptive," both in a single sentence:

However, there are some materials of this period [the late Middle Pleistocene] that fall outside, but not far outside, the strictest definition of Homo sapiens as based on the living species. Most of these (for example, Border Cave 5, Boskop, Fish Hoek, Klasies River Mouth except for AP 6222, and maybe Cave of Hearths) form a generally poorly dated South African group in which cranial structure largely conforms to the modern Homo sapiens morphology except that, most notably, the bipartite brow and/or the inverted-T-shaped chin are lacking. Do such fossils represent distinctive and now extinct populations of Homo sapiens that lacked two or more of the most striking autapomorphies of the living species merely as a result of random (or even adaptive) population variation? Or did they belong in life to one or more distinctive reproductive entities whose histories did not impinge, at least biologically, on that of today's Homo sapiens? (Tattersall and Schwartz 2008:52, emphasis added)

The bolded sentence is important. Tattersall and Schwartz view adaptive and random variations as equivalent: small changes between populations that may occur even without the kind of significant isolation that would invite a taxonomic interpretation. They contrast these in the next sentence with "distinctive reproductive entities whose histories did not impinge." And they are correct; modern human populations have morphological differences as a result of both selection and drift, and their histories certainly have impinged on each other.

But it makes a difference whether selection or drift was the cause of changes, because selection is more powerful than drift. Weak selection can cause a level of morphological differentiation that would require long isolation by random drift alone. If selection were involved in African regional differentiation, there may be no reason to posit "distinctive reproductive entities whose histories did not impinge" -- in fact, their histories almost certainly would have impinged.

In other words, the relation of the pattern of features to the taxonomic status of the populations depends on the evolutionary forces that generated the pattern.

As Weaver and Roseman note, their hypothesis that modern human cranial form evolved neutrally depends on the pattern of evolution of different features, not the amount of evolution of any single feature. But the amount of evolution must still be explained; under their hypothesis, it must have occurred in small populations over a substantial period of time. In their hypothesis, the cranial differentiation of African late Middle/early Late Pleistocene fossils would have emerged during relatively long periods of parital or complete isolation. Under that hypothesis, Tattersall and Schwartz would be correct to place these fossils into different taxa, only one of which was ancestral to living people -- or at least principally ancestral, allowing for some small amount of hybridization and introgression.

In contrast, Lieberman's adaptive hypotheses are consistent with the evolution of modern human cranial morphology within a broader, larger population. Patterns of selection may explain the variation among the fossils. Today's humans may have emerged from a population with substantial cranial polymorphism. That scenario would seem to be consistent with the patterns described by Pearson -- in which modern human cranial variation does not standardize until very late, perhaps even Holocene times. Only selection could cause this kind of evolution within the large populations of the last 10,000 years, or even within the large populations of the last 70,000 years.

I picked this problem first, because it was the first to stand out to me in the papers. It does seem a fairly glaring contradiction. I don't expect the authors to have noticed the contradiction in advance; I think that they approach the question of human origins from fundamentally different viewpoints.

As you can tell, two of the papers are not concerned with the causes of evolution at all -- their aim is to map the pattern of morphological variation onto putative speciation events. But it seems to me that if we approach the fossil record with the idea that speciation is the major cause of such patterns, then we have already assumed how the evolution happened. It may not have escaped your notice that this is the major reason for disagreement about modern human origins: One group of authors wants to assume the conclusion, foreclosing further discussion.

I don't have any complaints about the papers that were chosen for the issue -- in fact, I'm interested in reading the current opinions of all these authors. So far, I would say that each paper is a well-written expression of its authors' ideas, and I appreciate having all that in one place.

But it does seem a little strange that a special issue devoted to modern human origins in Africa doesn't have more, um, diversity of opinion. Several of the papers discuss multiregional evolution. They apparently believe that it is an important enough viewpoint to include their reasons for disbelieving it. One of the papers (Weaver and Roseman) includes a section about genetic introgression, kindly citing my work. Another (Bräuer) claims that it is reasonable to include all Middle Pleistocene humans in Africa and Europe as part of "one polytypic species, Homo sapiens" (Bräuer 2008:32).

So the work of those of us who write about evolutionary mechanisms seems to be making an impact. Still, it's kind of like "dark matter" -- you only know about the ideas because of their effects on what you can read! In this case, you can read a lot of peoples' opinions about these ideas -- you just can't read them from the people who thought of them.

What boring meetings these must be, with everybody agreeing with each other all the time, and nobody to point out all these contradictions!

References:

Bräuer G. 2008. The origin of modern anatomy: by speciation or intraspecific evolution? Evol Anthropol 17:22-37. doi:10.1002/evan.20157

Lieberman DE. 2008. Speculations about the selective basis for modern human cranial form. Evol Anthropol 17:55-68. doi:10.1002/evan.20154

Pearson OM. 2008. Statistical and biological definitions of "anatomically modern" humans: Suggestions for a unified approach to modern morphology. Evol Anthropol 17:38-48. doi:10.1002/evan.20155

Tattersall I, Schwartz JH. 2008. The morphological distinctiveness of Homo sapiens and its recognition in the fossil record: Clarifying the problem. Evol Anthropol 17:49-54. doi:10.1002/evan.20153

Weaver TD, Roseman CC. 2008. New developments in the genetic evidence for modern human origins. Evol Anthropol 17:69-80. doi:10.1002/evan.20161