Middle Pleistocene

Due to Jerry Coyne, I encountered an interview in the Guardian with Colin Blakemore: "Colin Blakemore: How the human brain got bigger by accident and not through evolution."

The headline is a misnomer, as Blakemore is not denying evolution, he is denying selection. But Blakemore's argument is based completely on a false presentation of the facts. Consider:

The question is: why is it so big compared to the brains of our predecessors, such as Homo erectus? Until 200,000 years ago, there had been a gradual increase in brain size among hominins, starting three million years ago. Then, abruptly, there was a remarkable increase of about 30% or so.

That's Blakemore. Now, here's a chart of endocranial volumes of Pleistocene human fossils:

Endocranial volume against time for fossil Homo.

Time is in thousands of years before present, running left to right.

As you can see, there's no sudden jump 200,000 years ago, or at any other time. The data, such as they are, are consistent with a single pattern of increase over time, as pointed out by Sang-Hee Lee and Milford Wolpoff (2003).

Heck, it's the lack of a sudden jump that has gotten all the attention. Because if "modern" humans suddenly showed up in Africa 200,000 years ago, and all of a sudden had vastly larger brains than any other hominins, wouldn't that be a simple and tidy story? Don't you think we'd all be talking about the sudden origin of modern humans as reflected by their larger brains?

It just didn't happen.

Well, it's one thing to be empirically wrong. That's a simple error that's easily corrected. But Blakemore, relying on the erroneous assumption of a single shift in brain size, asserts that neutral macromutations must be an important mode of human brain evolution:

Genetic studies suggest every living human can be traced back to a single woman called "Mitochondrial Eve" who lived about 200,000 years ago. My suggestion is that the sudden expansion of the brain 200,000 years ago was a dramatic spontaneous mutation in the brain of Mitochondrial Eve or a relative which then spread through the species. A change in a single gene would have been enough.

I hope that the empirical pattern is enough to convince you that this hypothesis is false. The "sudden increase" simply did not happen.

But in case you need more persuasion: Blakemore here assumes that the increase in brain size had no negative consequences. Otherwise it couldn't proceed neutrally. Here is his argument:

The environment of early humans was so clement and rich in resources that this greedy new brain, which would have absorbed even more of the body's energy, could be sustained without danger. Later, when times got hard, during droughts or climate changes, it helped us deal with these crises, which could otherwise have killed us off, by dreaming up novel ideas to problems.

You see the outline: Life was easy, and humans could grow fat-brained, like so many sheep. Fortunately, our fat brains were then useful when times were tough. Blakemore describes this as somehow different from the idea that brains were adaptive -- it's in fact just another adaptive story for larger brains.

But it falls apart, when we consider that assumption -- life was easy. I put it to my students this way: Suppose you lay a lot of sugar beets out on your land. What will happen to the deer population?

The answer is not that the deer will grow fat-brained and later evolve to conquer humanity. The answer is that there will be a lot more deer.

Population growth is much faster than adaptation, and it's hundreds of times faster than a neutral gene can transit through the population. Humans in the past were not a static population, living in peace with an abundant environment. They were repeated faced with Malthusian crises -- on submillennial timescales. That's why a close understanding of climate variability is so relevant to our evolution. The fact that tools and behaviors change so slowly in the Middle Pleistocene is informative -- it shows that humans weren't coming up with dramatically new ways to track shifting ecologies.

And that means that the selection pressures of the energetic and life history constraints on the brain were repeatedly imposed on human populations. A substantial increase in brain size should have immediately been disadvantageous -- if it had no compensatory benefits to fitness.

What remains is testing the hypotheses about those benefits to fitness. Blakemore actually is presenting one such hypothesis -- that a larger brain mostly was adaptive because of its ability to transmit traditions. That's testable, and is consistent with the greater transfer of information apparent in recent archaeological traditions compared to Middle Pleistocene ones. But there are other hypotheses as well, and it is quite difficult to compare them with the available record.

That's why it's so important to state the empirical record accurately.

UPDATE (2010-03-29): A reader points out that Malthusian crises, in terms of resource or food availability, may have been avoided by warfare or predation -- people kill each other instead of starving. I see that point, particularly where we consider the way that epidemic disease can relax competition for food until population growth resumes. Performing well under predation or competition would be one way that brain size might have had compensatory benefits to fitness beyond its energetic and life history costs.

References:

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

I wrote about Crete twice last month ("Crete: Pleistocene port of call?", "More tools from Crete"). Now John Noble Wilford writes about Strasser and Panagopoulou's work: "On Crete, New Evidence of Very Ancient Mariners". The article reviews the finds, and then gives space to a bunch of speculations.

The exposed uplifted layers represent the sequence of geologic periods that have been well studied and dated, in some cases correlated to established dates of glacial and interglacial periods of the most recent ice age. In addition, the team analyzed the layer bearing the tools and determined that the soil had been on the surface 130,000 to 190,000 years ago.

Dr. Runnels said he considered this a minimum age for the tools themselves. They include not only quartz hand axes, but also cleavers and scrapers, all of which are in the Acheulean style. The tools could have been made millenniums before they became, as it were, frozen in time in the Cretan cliffs, the archaeologists said.

Dr. Runnels suggested that the tools could be at least twice as old as the geologic layers. Dr. Strasser said they could be as much as 700,000 years old. Further explorations are planned this summer.

Ancient artifacts may be exposed to the elements once again and then re-incorporated into more recent sedimentary contexts, a process called "reworking". It happens. But it's a stretch, unless there is some independent evidence that the tools and surrounding rocks bear signs of battering from water transport or other contextual evidence of reworking.

Going out and saying that the tools could be "as much as 700,000 years old" is just overreaching -- it's like they're trying to say this is comparable to the "earliest" evidence of watercraft. And you really have to stretch the dates to get there: Flores was apparently inhabited by 800,000 years ago.

At the end:

But archaeologists and experts on early nautical history said the discovery appeared to show that these surprisingly ancient mariners had craft sturdier and more reliable than rafts. They also must have had the cognitive ability to conceive and carry out repeated water crossing over great distances in order to establish sustainable populations producing an abundance of stone artifacts.

Maybe. Maybe not. What evidence is there that the crossings were "repeated"? Imagine what would serve...finding Crete-derived rocks in a mainland site would do it, or vice-versa. Any evidence of transport. I don't imagine we'll find any earlier human-introduced fauna, and a human-induced extinction might result from a single invasion, not a "sustained" record of multiple crossings.

I pointed to one such faunal turnover in my last Crete post, which would point to a human invasion in the mid-Middle Pleistocene. Parallel technical change with Greece or North Africa after this time would show multiple contacts -- but such evidence would suppose a long archaeological record that we don't yet have.

I just don't think it helps to speculate so freely. Sure, we might find things that surprise us. But the actual facts are surprising enough to justify funding much more work.

Bruce Bower reports on excavations by Thomas Strasser on the Mediterranean island of Crete: "Ancient hominids may have been seafarers".

At Preveli Gorge, Stone Age artifacts were excavated from four terraces along a rocky outcrop that overlooks the Mediterranean Sea. Tectonic activity has pushed older sediment above younger sediment on Crete, so 130,000-year-old artifacts emerged from the uppermost terrace. Other terraces received age estimates of 110,000 years, 80,000 years and 45,000 years.

These minimum age estimates relied on comparisons of artifact-bearing sediment to sediment from sea cores with known ages. Geologists are now assessing whether absolute dating techniques can be applied to Crete’s Stone Age sites, Strasser says.

I would set a high bar for evidence on this one. No details are available; it was a conference presentation.

One possibility: According to Alexandra van der Geer and colleagues (2006), there was a faunal turnover on Crete 300,000 years ago. The earlier fauna included a 1.5-meter dwarf mammoth and dwarf hippos. The hippos were hoof-walkers apparently adapted to a "more terrestrial" activity pattern. Sometime after 400,000 years ago, this fauna was replaced. No more hippos or mammoths, and new, larger, mainland-derived elephants. As they wrote (125):

The dwarf elephant may be large compared to the mammoth of the previous period, but it is still about 30% smaller than its mainland ancestor E. antiquus, which has a shoulder heigth of 3.7 m. The dwarf elephant has strongly curved tusks. It is still a matter of debate why this elephant did not reach a pygmy size.

The arrival of humans is one possibility. Sondaar and van der Geer (2002) suggested that Sardinia-Corsica might have undergone similar turnovers induced by human arrivals during the Middle and Late Pleistocene.

But that's entirely speculation. I want to see some dating and good descriptions of the artifacts and their context.

If the artifacts found by Strasser represent a genuine occupation, the Cretans would presumably have been seafaring Neandertals. Or Preneandertal-derived hobbits. Man, I wish I'd made that one of the 2010 predictions!

References:

van der Geer A, Dermitzakis M, de Vos J. 2006. Crete before the Cretans: The reign of dwarfs. Pharos: Journal of the Netherlands Institute in Athens 13:119-130.

Sondaar PY, Van der Geer AAE 2002. Plio-Pleistocene terrestrial vertebrate faunal evolution on Mediterranean islands, compared to that of the Palearctic mainland. Annales Géologiques des Pays Helléniques 1e Série 39, A: 165-180.

In Science this week, Nira Alperson-Afil and colleagues report on recent excavations at Gesher Benot Ya'aqov, Israel. I saw some of this research presented at a conference, and I thought it was quite amazing to see the preservation of organic materials at this site. The Science paper is a good summary of the high points, presented in a very readable way.

About the site:

Gesher Benot Ya’aqov is located on the shores of the paleo–Lake Hula in the northern Jordan Valley in the Dead Sea Rift (7). The Early to Middle Pleistocene sediments document an oscillating freshwater lake and represent some 100,000 years of hominin occupation (Oxygen Isotope Stages 18–20) dating to 790,000 years ago (8, 9). Fourteen archaeological horizons indicate that Acheulian hominins repeatedly occupied the lake margins, where they skillfully produced stone tools, systematically butchered and exploited animals, gathered plant food, and controlled fire (7, 10–15).

The current paper reports on a single occupation level, characterized by a hearth feature and associated plant, animal, and artifactual remains. Some interesting things:

1. The plant remains:

Although most taxa indicate wet habitats (e.g., lakes, lake margins, swamps, and near streams), the abundant fruit remains of woodland species such as olive, oak, and officinal storax (Styrax officinalis) imply human involvement, as their habitat was likely located some distance from the lake shore. Edible plants include oak acorns, prickly water lily (Euryale ferox) seeds, and water chestnut (Trapa natans) fruits; these were probably staple foods because of the nutritive value of their starchy nuts. Through roasting, the inedible shell of the nuts can easily be peeled and the tannin content of the acorns reduced. The fruits of the wild grapevine (Vitis sylvestris) and olive, and the leaves of the white beet (Beta vulgaris) and holy thistle (Silybum marianum), may also have been consumed.

2. Crabs:

The 17 crab specimens [minimum number of individuals (MNI) = 4 (22)], identified as the extant Potamon potamios, include pieces of the two asymmetric chelipeds, each with a distinctive form of the movable (upper) and fixed (lower) pincer....Of the seven pincers of the large cheliped present in Level 2, six occur around the hearth. These are the only crab remains in this area (fig. S4) (23).

What's not to like about people eating crabs?

3. Spatial patterning. There are two distinct areas of the horizon with anthropogenic activities -- the hearth and a second cluster of tools and stone waste flakes, I'm not very excited about the spatial distribution of activities. The story in the news is about how ancient humans knew how to "keep house" -- they're selling it as a major breakthrough in cognitive evolution.

But the reason why we rarely have archaeological evidence about spatial patterning is that an archaeological horizon doesn't have very good temporal resolution. Here's an alternative scenario to account for the spatial pattern of remains in this horizon: One day, some people came, made tools and ate some fish. Three weeks later, some other people were in the same area, and they stayed for a few days, made a fire, did a bunch of other stuff.

That's pretty much the spatial pattern that I would find if I went back home to Kansas and checked out campsites around the shore of the local reservoir. Few campsites are occupied for very long, and different people use them over time, sometimes with a fire, often not. Sure, we're cognitively advanced. I'm just not convinced that the spatial distribution of our campsite trash is very good evidence about it.

Here's what the paper includes about the spatial patterning:

The evidence from Gesher Benot Ya’aqov suggests that early Middle Pleistocene hominins carried out different activities at discrete locations. The designation of different areas for different activities indicates a formalized conceptualization of living space, often considered to reflect sophisticated cognition and thought to be unique to Homo sapiens (3). Modern use of space requires social organization and communication between group members, and is thought to involve kinship, gender, age, status, and skill (2).

I think this is weak on two grounds -- first because the archaeology is poor evidence about the formal conception of living space, and second because it's not obvious that there's anything very unique about it.

Why not unique? Any animal that can make a structure must have some capacity to pattern spatial activities -- if they don't, there's going to be poop everywhere. Conditioned on the fact that a human social group is sharing a single space, and group members are doing more than one activity, I don't see how you would ever expect to find a uniform scatter of evidence of these activities. There will always be some kind of spatial pattern, from the mere fact that two people can't occupy the same space at the same time.

Remember that Gesher Benot Ya'aqov provides the earliest good evidence of human-controlled fire. It's no coincidence that "spatial patterning" should be found with a fire -- anything that people did anywhere other than by the fire is automatically evidence of a pattern.

4. Fish. Now if there is one big reason why the spatial patterning is useful, it's the interpretation of the fish remains. It's not in the least bit surprising that there would be a lot of fish remains on an ancient lakeshore. But the remains are clustered into two distinct parts of the site, which happen to be the very two locations that humans were clearly using.

In other words, once you accept that the archaeology gives you some evidence of where the people were within the site, you can test for association of the fauna and plant remains with the people. The crabs aren't all around the fire because of a failed attempt to stay warm at night; the people brought them there and ate them. The fish remains are clustered around the fire and flintknapping areas because people were eating them.

Here's a good moral of the Gesher Benot Ya'aqov story: It's now past time to stop talking about whether "pre-modern" humans used aquatic resources. They did, sometimes intensively. I never understood why this argument about seafood and modern humans ever got any traction. We've known for twenty years that coastal Neandertals ate shellfish. We also have known from the numbers in caves near the coast that people never seem to have transported them very far inland. So there was a good reason why you didn't see more evidence of seafood; there just weren't that many sites very near the coast.

So why was it news when a bunch of coastal African sites started producing evidence of shellfish consumption? Evidence that we already had for coastal Neandertals? I don't understand. Well, here we have people eating crabs and lots and lots of fish, 800,000 years ago. We can add the paper by Jose Joordens and colleagues earlier this year about Trinil (I reviewed it in "The shells of Trinil"), a million years ago or more.

Another reason why Gesher Benot Ya'aqov is interesting: outside Africa, Middle Pleistocene sites (and Late Pleistocene sites, for that matter) have a fairly extreme bias toward caves and rock shelters. Caves can preserve evidence of within-site spatial patterns, and certainly offer some exceptional opportunities to track human activity over long periods of time. However, humans aren't very likely to have schlepped hundreds of fish from a lakeshore into some remote cave.

UPDATE (2009-12-18) Thanks to a reader who pointed out a hanging omission; I corrected the text.

References:

Alperson-Afil N, Sharon G, Kislev M, Melamed Y, Zohar I, Ashkenazi S, Rabinovich R, Biton R, Werker E, Hartman G, Feibel C, Goren-Inbar N. 2009. Spatial Organization of Hominin Activities at Gesher Benot Ya’aqov, Israel. Science 326:1677-1680. doi:10.1126/science.1180695

A week or two ago, I was pointed by a press release to some recent research from Bolomor Cave, Spain, where the levels occupied by early/pre-Neandertals have been yielding interesting evidence about diet breadth. The pointer was about "bird consumption", but in this case the birds are all ducks -- genus Aythya, which includes living canvasbacks, for you duck hunters out there. The reference is a newish paper in Journal of Archaeological Science by Ruth Blasco and Josep Fernández Peris.

Something like 155,000 years ago, some hominins brought 8 ducks into the cave, cut them up (leaving cutmarks) and roasted some of them (leaving bone with burned and charred ends where the meat isn't).

Not so terribly surprising, but then we don't have a lot of sites of equivalent age where there's good evidence of repeated bird consumption. The cave also has a lot of rabbit bones, and some tortoises.

Blasco (2008) described the evidence for tortoise consumption from a somewhat later level of the cave (Level IV), dating to before 121,000 years ago. That paper included the gruesome work of identifying human toothmarks that gnawed off the ends of several of the long bones. They also roasted some of the tortoises, apparently before disarticulation.

What I found an interesting element of both papers was the close analysis of the application of fire in the processing of the remains. Naturally from this distance in time it isn't possible to discover everything. But together with experimental archaeology and taphonomy, it may be possible in many cases to test for the presence of ethnographically-attested models of butchering, cooking, and post-consumption processing of the remains.

This means that where the record is good, you can also test for the absence of such behaviors. I was reminded last week that I haven't yet posted my review of Richard Wrangham's book, Catching Fire. In light of several requests, I'm buffing off the rough edges now and I'll post it later this week. When it comes to testing Wrangham's hypothesis -- in brief, that "cooking made us human" -- it is precisely the kind of close archaeological work pursued in these papers that is necessary.

Which makes it interesting that, in these rather recent archaeological levels with clear evidence of cooking, there is good evidence that several of the ducks and tortoises weren't cooked before humans ate them.

References:

Blasco R. 2008. Human consumption of tortoises at Level IV of Bolomor Cave (Valencia, Spain). J Archaeol Sci 2839-2848. doi:10.1016/j.jas.2008.05.013

Blasco R, Fernández Peris J. 2009. Middle Pleistocene bird consumption at Level XI of Bolomor Cave (Valencia, Spain). J Archaeol Sci 36:2213-2223. doi:10.1016/j.jas.2009.06.006

Scott and Gibert report in today's Nature on the "oldest handaxes" in Europe:

In Africa, large cutting tools (hand-axes and bifacial chopping tools) became part of Palaeolithic technology during the Early Pleistocene (1.5 Myr ago). However, in Europe this change had not been documented until the Middle Pleistocene (<0.5 Myr ago). Here we report dates for two western Mediterranean hand-axe sites that are nearly twice the age of the supposed earliest Acheulian in western Europe. Palaeomagnetic analysis of these two sites in southeastern Spain found reverse polarity magnetozones, showing that hand-axes were already in Europe as early as 0.9 Myr ago. This expanded antiquity for European hand-axe culture supports a wide geographic distribution of Palaeolithic bifacial technology outside of Africa during the Early Pleistocene.

The "Anthro 101" version of the Acheulean makes it out to be a million-year-long technological yawn. The breakthrough of the first handaxes 1.5 million years ago led to a stultifying stasis. The handaxe was a "Paleolithic pocket knife" useful for many purposes -- but the advent of Levallois manufacture around 300,000 years ago consigned the handaxe to the midden of history. Except, of course, for scattered, benighted peoples who were still using handaxes up into historic times -- the exceptions proving the rule of bifaces' never-ending utility.

Well, the Acheulean was boring, but it wasn't uniform. The Anthro 101 version makes Acheulean people sound too accomplished -- like they invented the bifaces and then started turning them out like industrial robots for a million years.

Not so: Fine, finished bifaces tend to be less than 500,000 years old. They also tend to be European. Acheulean people didn't usually carry rock very far. With more sources of chert and flint, Europe's geology allowed a wider selection of fine handaxes than Africa's. That is, at least after 500,000 years ago or so. Before then, there just weren't very many handaxes in Europe.

Here, Scott and Gibert suggest that maybe some other sites with "advanced" or "terminal" Acheulean may prove to be earlier than people now think. The two sites in this study were both initially thought to be much later -- for example:

The youthful age (200 kyr old) assumed for Solana del Zamborino was largely based on its well-developed Acheulian lithic typology. Such a young age contrasts with our continuing lithostratigraphy and palaeoclimate research in the region, which indicates a final, major lake-forming event near the end of the Early Pleistocene (starting 800 kyr ago) and deposition terminating in the Baza Basin (600 kyr ago).

They could well be right -- some European sites now thought to be late (post-500 kyr) might be earlier. What does that mean for our understanding of the Acheulean?

Lower Pleistocene Europeans sometimes made finished bifaces, these were initially sporadic, and later became more and more common until the advent of Middle Paleolithic technocomplexes. The sporadic appearance suggests that people could live without handaxes, and that they were simple enough to be repeatedly invented. There's just not that much information content there, and groups of Early to Middle Pleistocene people arrived at the same solutions again and again.

Technological "progress" is a misnomer before around 300,000 years ago. Early Homo made Oldowan (and Oldowan-like) industries that required few capabilities not mastered routinely by wild chimpanzees. Some, sure, but few. Bifaces require a bit more: a spatial conception of symmetry, longer action sequences. But Early and Middle Pleistocene people didn't carry it off all the time; they kept losing the biface outside Africa. And they kept hitting that biface mode. Curious.

Other entries of interest:

"Early Malaysian axes

And then there was Levallois

How monolithic was the Acheulean?

Acheulean endings

References:

Scott GR, Gibert S. 2009. The oldest hand-axes in Europe. Nature 461:82-85. doi:10.1038/nature08214

Fed up on hobbit news? Well, I'm going to do my best this week to scoop the science journalists, covering stories in paleoanthropology that ought to get some more attention but might be drowned out by otherwise hobbitrocious stories.

I'll start with a story in which I have a special interest -- a new paper by Jeff Wall, Kirk Lohmueller, and Vincent Plagnol, titled, "Detecting ancient admixture and estimating demographic parameters in multiple human populations."

A couple of years ago, Wall and Plagnol (2006) looked at a sample of genes in the "Environmental Genome Project. At that time, the sample consisted of 135 genes in 12 Yoruba and 22 CEPH individuals. It's not a large sample by today's 3.9-million genotype standards. But the EGP sample has one important thing going for it -- with resequencing data, we have access to a much larger number of mutational differences at very small map distances from each other. Tight linkage between sites means that we can use the genealogical properties of samples to examine much more ancient events. The HapMap gives us a vast number of genotypes from a large sample of individuals, but the density of loci is quite low -- an average of nearly 1000 base pairs between loci. The EGP doesn't sample as many loci, but it gives a denser representation of the variation at each locus. Only this kind of sample is sufficient to test for genetic ancestry of modern human populations in ancient populations of the Middle Pleistocene.

Plagnol and Wall applied a simple admixture model to these data, and found that the complete out-of-Africa replacement model did not adequately explain the variation in the European-derived sample. Instead, they found that a model with 5 percent admixture of some non-African Middle Pleistocene ancestral population was a much better fit for the current diversity of European gene trees. In other words, the low variation of recent humans cannot be explained by a small population in a single ancient population; instead, there must have been several populations, partly isolated from each other, one or more of which gave regionally-specific alleles to modern Europeans. Multiregional evolution fits those observations very well -- this is not one or two introgressive genes, and there is no specific evidence of selection on them (although selection may be responsible).

A number of people picked up on that study in the course of later work. Gregory Cochran and I discussed it in our own 2006 paper about genetic introgression. In late 2005, Dan Garrigan and colleagues had published their own analysis of a pseudogene region on the X chromosome, called RRM2P4. Garrigan reviewed this work together with Mike Hammer (2006) and again with Sarah Kingan (2007). Early last year, I also reviewed the evidence together with Cochran, Henry Harpending and Bruce Lahn (2008).

We and many other people are following up on this research, trying to discover the ancestry of human populations beyond the simple out-of-Africa replacement scenario. In the new study, Wall and colleagues extend their analysis to a more recent release of the EGP, including 222 genes, and adding 24 Chinese individuals to the 12 Yoruba and 22 CEPH individuals. It's a simple paper and relatively short. In a word, they find that their data reject the simple out-of-Africa replacement scenario, and that the genetic variation of coding genes in their sample must be explained in part by long-standing population structure.

It's not proof that the Neandertals, or any other particular group of ancient humans, survived and passed their genes on to more recent people. This is a study of the genes of recent human populations, and it merely concludes that their ancestors could not have lived in a single small population. Maybe every Neandertal became extinct, and present-day Europeans got this genetic variation from somewhere else. But it is logical to figure that non-Afircan populations may have been among the contributors to present non-African peoples -- particularly since the statistical test focuses on region-specific gene frequencies. The study also finds evidence that today's African population has a complex ancestry -- a kind of multiregional scenario playing out inside Africa (or potentially involving gene flow back into Africa from elsewhere).

Testing for admixture

Wall and colleagues reasoned that an allele coming in from an ancient, partially isolated human population would vary in a distinctive pattern. Because of the long history of partial isolation in an ancient subpopulation, they expected that such an allele would come in with multiple mutational differences from the non-introgressive allele. And if it came in from some non-African population, it ought to show relatively strong differences in frequency between populations. So they devised a statistic, mathematically combining F_ST and a linkage measure -- the idea being to detect alleles that differentiate populations and that are surrounded by large sets of tightly linked polymorphisms.

This kind of pattern might also occur under positive selection. But a new mutation under positive selection would start out weakly linked to nearby polymorphisms, each of which already exists at some substantial frequency in the population. An introgressive allele might be linked to several other unique mutations that happened during the long period of limited gene flow between ancient populations. And a new mutation would not tend to be surrounded by high F_ST polymorphisms, until it got to be very common in the population -- up above 50 percent. In contrast, an introgressive allele coming into the population with several nearby mutations would generate a cluster of relatively high F_ST polymorphisms even at low frequencies. It may not be a perfect test for any individual locus -- there's a lot of uncertainty. But applied to more than 200 loci, it should be possible to test the hypothesis that "archaic admixture" is zero.

Wall and colleagues do test that hypothesis, and they are able to refute it strongly for each of the three groups. Living European and Chinese samples refute the out-of-Africa replacement model with p<0.01. The Yoruba sample refutes the hypothesis of panmixia in ancient Africans at p<0.0000001.

The authors also provide a supplementary table with a list of genes that may be candidates for introgression. I didn't see any really obvious genes on the list, but each of them bears some examination. I expect that we will be able to use more detailed analytical techniques to look at the regions around these genes and see what is going on. Or at least, in the next couple of years more and more resequencing data will become available, allowing us to test the same hypotheses with larger samples.

It's worth pointing out that nothing in the approach of Wall and colleagues implies that any of the putative introgression occurred under natural selection. I've argued that introgression may have occurred under selection in ancient humans, but so far few other people have looked at the question with the idea of ancient selection in mind. No doubt we can improve a bit on the methods in the paper if we are willing to make some assumptions about the evolutionary dynamics involved in Late Pleistocene populations.

Lingering uncertainty

So what's not to like about this study? After all, here we have what appears to be strong evidence against an exclusive out-of-Africa replacement. It suggests that the ancestry of recent Europeans and Asians owes something to the Middle Pleistocene populations of those regions, and gives an estimate of that contribution consistent with what we know so far about the Neandertal genome.

But I have to approach this study as critically as I would any other piece of population genetics. In this case, there is a clear weakness to their model. The authors tested for significance of a single parameter, which they call "archaic admixture." Consider their Figure 1, a schematic of their population model:

Is "archaic admixture" significantly different than zero? Well, you can see that must depend on the values of no less than six other parameters. When did the European population start growing significantly -- was it after the Last Glacial Maximum? During the Neolithic? The Aurignacian? How about the African population? Was there really a long bottleneck in the ancestry of Europeans?

The reason why I'm so critical of population models used in genetics is simple. The authors of studies almost never try to make the simplest effort to justify these kinds of parameters against the archaeological or fossil record. Their conclusions -- in this case, the significant finding of ancient admixture -- depend on some range of values for these other parameters.

Now, Wall and colleagues take a fundamentally different approach than I would use. I would draw upon non-genetic sources of information about these parameters, to increase confidence about the others. In contrast, they performed a broader range of simulations, attempting to find maximum likelihood estimates for all the parameters simultaneously.

The problem with that approach is that it's hard to say that some other parameters may not have been more important. Consider recent positive selection. As I mentioned above, a recent positively selected mutation could in principle create a pattern like that described for an introgressive allele -- at least under the statistics used in this paper. The chances are low for any randomly chosen mutation under positive selection, because a new positively selected mutation isn't likely to be linked to other rare mutations -- it's much more likely to be linked to common polymorphisms. But if we actually have many hundreds, or even thousands, of recently selected alleles (as we do in humans), then there is a pretty good chance that some of them will look like introgression under the test used here. Another scenario that could mimic introgression under this statistical approach is long-standing balancing selection.

There are probably too many genes on these lists for all of them to reflect selective balances or recent positive selection -- there are a lot of recently selected genes, but few of them will have the specific kind of linkage that would show up as significant in this study. But I think the authors could do more to validate the demographic model against non-genetic evidence. Besides that, there is plenty of morphological evidence for gene flow among these ancient human populations. The authors would be well-served to work more directly with the morphological record of human evolution -- when they write that:

To our knowledge, the question of ancient admixture in other parts of the world has been relatively neglected by the evolutionary genetics community

it is both true and sad. There is abundant anatomical evidence addressing the issue of genetic continuity or gene flow in parts of the world other than Europe.

UPDATE (2009-05-08): Dienekes also looks at the paper, and suggests that finding evidence for ancient population structure in Europe and East Asia may be no big deal, because it may simply derive from population structure within Africa before the putative out-of-Africa migration. I'd have to review the data to be sure, but it seems to me there are two arguments against that explanation:

1. The East Asian and European comparisons come up with different genes showing evidence of putative introgression. There's not a lot of overlap between the sets. If this were merely ancient East African genes, we'd expect the populations outside Africa to have the same ones. And the numbers had actually been cut down by the serial founder effect scenario (Chinese having undergone more and larger bottlenecks), then we'd expect China to have a subset of the European introgressive genes. I wouldn't go out on a limb about this without looking at the actual frequencies of the supposed ancient alleles, but the pattern isn't consistent with Europe and China being drawn randomly from the same ancient African population.

2. The entire point of the out-of-Africa replacement idea is to draw humans from an unstructured ancient population. Humans have to be inbred to explain the low genetic variation today. A long bottleneck in Africa is one explanation for this inbreeding -- but the bottleneck has to have been severe, down to an effective size around 10,000, and it has to be very long. A long history of population structure within Africa works against that bottleneck -- population structure featuring several partially isolated populations would prevent the kind of inbreeding that a long bottleneck could create. If Wall and colleagues are correct, we would have to scrap the long bottleneck idea and come up with some other explanation for high inbreeding. There are some others, as I've pointed out before.

There are other arguments against exclusive continuity outside Africa, and in favor of some significant -- perhaps overwhelming -- gene flow from Africa into the rest of the world during the late Pleistocene. But no other argument is exclusive of some continuity outside Africa. And if we don't need the bottleneck anymore, accepting some continuity is the reasonable explanation for the facts that don't fit, including the observations in this paper and the morphological and archaeological evidence suggesting continuity.

References:

Evans PD, Mekel-Bobrov N, Vallender EJ, Hudson RR, Lahn BT. 2006. Evidence that the adaptive allele of the brain size gene microcephalin introgressed into Homo sapiens from an archaic Homo lineage. Proc Nat Acad Sci doi:10.1073/pnas.0606966103

Garrigan D, Kingan SB. 2006. Archaic human admixture: A view from the genome. Curr Anthropol 48:895-902. doi:10.1086/523014

Garrigan, D., Mobasher, Z., Severson, T., Wilder, J. A., Hammer, M. F. 2005b. Evidence for archaic Asian ancestry on the human X chromosome. Mol. Biol. Evol. 22:189-192. doi:10.1093/molbev/msi013

Hardy, J., Pittman, A., Myers, A., Gwinn-Hardy, K., Fung, H. C., de Silva, R., Hutton, M. and Duckworth, J. 2005. Evidence suggesting that Homo neanderthalensis contributed the H2 MAPT haplotype to Homo sapiens. Biochemical Society Transactions 33:582-585.

Hawks J, Cochran G. 2006. Dynamics of adaptive introgression from archaic to modern humans. PaleoAnthropology 2006:101-115. Open access

Hawks J, Cochran G, Harpending HC, Lahn BT. 2007. A genetic legacy from archaic Homo. Trends Genet doi:10.1016/j.tig.2007.10.003

Plagnol, V., Wall, J. D. 2006. Possible ancestral structure in human populations. PLoS Genet. 2:e105. doi:10.1371/journal.pgen.0020105

Wall JD, Lohmueller KE, Plagnol V. 2009. Detecting ancient admixture and estimating demographic parameters in multiple human populations. Mol Biol Evol (early online) doi:10.1093/molbev/msp096

Zietkiewicz, E., Yotova, V., Gehl, D., Wambach, T., Arrieta, I., Batzer, M., Cole, D. E., Hechtman, P., Kaplan, F., Modiano, D., Moisan, J. P., Michalski, R., Labuda, D. 2003. Haplotypes in the dystrophin DNA segment point to a mosaic origin of modern human diversity. Am. J. hum. Genet. 73:994-1015.

Hebrew University has issued a press release about ongoing research on human and animal bones from the Jericho excavations. They're looking for signs of tuberculosis:

While the origins of tuberculosis and its evolution remain unclear, it is thought it came from the first villages and small towns in the Fertile Crescent region about 9-10,000 years ago. Jericho is one of the earliest towns on earth, dating back to 9,000 B.C., and so a lot of communicable - or town - diseases would have had a good start in this community.

By examining human and animal bones from this site, the researchers will be able to see how the first people living in a crowded situation developed the diseases of crowds and how this affected the disease through changes in DNA -- of both the microbes and the people.

The most significant results of this research will come from a comparison between those data for humans and corresponding animal remains which may allow the identification of animal-human vectors and their interaction.

That's all very interesting, and looking for newly-virulent versions of tuberculosis in Neolithic bones is not a bad idea. But somebody ought to tell them that the zoonosis hypothesis (that tuberculosis was recently derived from domesticated animals like cattle) looks a lot less likely, now that ancient strains of the pathogen up to 3-million-years old have been found in living people, and signs of the disease have been found in a Middle Pleistocene human.

Anyway, that doesn't refute the idea that major changes in the pathogen population may have happened with human population growth, as new large reservoirs of people emerged. And it's quite possible that the germ went from humans to some of its animal hosts at that time, so studying the animal bones may give some information about the event. But they'll want to start with the idea of diversity within humans, not the other way around.

UPDATE (2008/4/15): The presentation was withdrawn from the meetings. I'm told that the information in the abstract is accurate, and that the withdrawal doesn't concern the science...

And no, the room wouldn't have been nearly big enough...

ORIGINAL POST:

Just flipping through the abstracts volume...this looks interesting:

New Homo erectus crania from Ethiopia

Simpson, S. W., Semaw S., Quade, J., Levin, N. E., Butler, R., Rogers, M. J., Holloway, R. L., Renne, P. R., Dupont-Nivet, G., Stout, D., Everett, M.

By the Early Pleistocene, members of the genus Homo were distributed throughout Africa and Asia, spreading into Europe by the Middle Pleistocene. As expected from such a widely distributed and long-lived species, variation in anatomical details is marked. This variation has fueled debate about the number of Early Pleistocene Homo species that existed and their relationship with modern humans. Here we report on two newly discovered hominid adult crania - one female and one male - dated to 1.5-1.7 My from the Busidima Formation, Gona Paleoanthropological Research Project area, Afar State, Ethiopia. An additional H. erectus cranial fragment (˜1.24My) is also reported. These crania are near contemporaries of specimens from Kenya, Tanzania, Republic of Georgia, and Southeast Asia and are attributable to Homo erectus. These fossils document a greater degree of brain size variation than previously known and allow a better accounting of the magnitude and character of cranial sexual dimorphism in size and shape.

New fossils, "greater degree of brain size variation," very cool. I hope they have a big enough room.

OK, I'm clearly going to have to cut out the beer if I'm going to do anything about stories like this one:

New research led by UC Davis anthropologist Tim Weaver adds to the evidence that chance, rather than natural selection, best explains why the skulls of modern humans and ancient Neanderthals evolved differently. The findings may alter how anthropologists think about human evolution.

Weaver's study appears in the March 17 issue of the Proceedings of the National Academy of Sciences. It builds on findings from a study he and his colleagues published last year in the Journal of Human Evolution, in which the team compared cranial measurements of 2,524 modern human skulls and 20 Neanderthal specimens. The researchers concluded that random genetic change, or genetic drift, most likely account for the cranial differences.

In their new study, Weaver and his colleagues crunched their fossil data using sophisticated mathematical models -- and calculated that Neanderthals and modern humans split about 370,000 years ago. The estimate is very close to estimates derived by other researchers who have dated the split based on clues from ancient Neanderthal and modern-day human DNA sequences.

The close correlation of the two estimates -- one based on studying bones, one based on studying genes -- demonstrates that the fossil record and analyses of DNA sequences give a consistent picture of human evolution during this time period.

"A take-home message may be that we should reconsider the idea that all morphological (physical) changes are due to natural selection, and instead consider that some of them may be due to genetic drift," Weaver said. "This may have interesting implications for our understanding of human evolution."

If you've been reading for long, you might reasonably wonder what I think about this study. My work has shown rapid natural selection in recent humans, consistent with evidence from recent skeletal samples for rapid evolutionary change. So it might seem incongruous that a study could assume that there has been no natural selection on the skeletal traits of recent human populations, and come to any kind of sensible conclusion.

I am actively working on this particular problem, with a manuscript in preparation, so I don't want to comment too extensively. However, I can say a brief word about why I disagree with the analysis.

A model of phenotypic evolution by genetic drift requires an assumption about the effective size of the population (N_e). Weaver et al. (2008) assume a model of "mutation-drift equilibrium." This is an assumption that the effective population size has not changed over time in the populations under consideration -- in this case, the Neandertal and human populations back at least as far as their common ancestor.

In their analysis, Weaver et al. (2008:4647) assume that the effective sizes of the human and Neandertal lineages, throughout the last few hundred thousand years, were equal to 2700 individuals. They wrote this:

The second reference point is the effective population size, PN_e, under a mutation-drift-equilibrium model for sub-Saharan African human populations. Zhivotovsky and colleagues (ref. 17) estimated N_e from 271 microsatellites using an equation equivalent to our Eq. 7 as ≈ 2,700 individuals. Once again, we are just assuming that the morphological and microsatellite estimates should match up under the same model, not that this is the most realistic model to use to infer the actual effective population size.

This is an astounding assumption. It is important because a small effective size allows rapid evolution by genetic drift. But it is contradicted by other evidence.

For one thing, most other sets of genetic data indicate a long-term effective size of at least 10,000 for human populations -- four times larger than assumed in this study. All things being equal, this means that the rate of phenotypic evolution by genetic drift should be four times slower than assumed by Weaver et al. (2008). Some of this difference between real and assumed effective sizes may be washed out by their process of calibration -- their equations involve several unknowns that must be simultaneously estimated, and give a lot of wiggle-room to the results. But that points to another weakness of the analysis -- there's so much wiggle room that almost any level of phenotypic difference might look like "drift."

Moreover, the human population has vastly increased in numbers within the last 50,000 years. Weaver et al. (2008) use the phenotypic and genetic divergences of recent humans to calibrate their "clock" of phenotypic evolution. But the phenotypic divergences between recent human populations, with very large effective population sizes (N_e > 100,000) are simply not comparable to those between Middle Pleistocene humans and Neandertals -- at least, not without taking into account the vast difference in effective population sizes.

But please don't take my word for it. I am a clear partisan on the side of natural selection in recent human evolution. Weaver's quote in the press release above implies that we should accept a pluralistic model, in which genetic drift accounts for some changes. I agree entirely. But their analysis assumes that genetic drift accounts for all changes. I don't deny the role of genetic drift, but I do deny that it explains much about recent skeletal evolution in humans. Random chance cannot do much in a very large population in a few hundred generations.

I really don't understand why you would want to use a heuristic value for effective population size, when it is contradicted by genetic and archaeological evidence. I will be writing about effective population size over the next week, introducing some of the importance of the concept for these kinds of analyses. You're welcome to take a look at what I have to say, and take it or leave it.

Edmund Blair Bolles is reporting from the Evolang conference in Barcelona. Unfortunately I had to cancel my presentation there, but it has been great to read these summaries of some of the papers. I wanted to point readers to his account of Francesco D'Errico's talk:

Neanderthals had language comparable to that of Homo sapiens, Bordeaux-based archaeologist Francisco D’Errico told participants in the Evolang conference in Barcelona this morning (Saturday, March 15, 2008). This claim totally discards the older Big Bang theory that said language arose only very recently (40 to 75 thousand years ago), and also challenges the Out-of-Africa theory that proposes Homo sapiens emerged in Africa about 200 thousand years ago and spread over the rest of the world, carrying language and culture with the, beginning about 60 thousand years ago. A new history will have to be written.

If you have been reading here, you have seen many of the new perspectives D'Errico is talking about, but together they make a very compelling package. Consider:

1. We now know that australopithecines had ape-like vocal tracts, complete with pharyngeal air sacs.

2. We now know that Middle Pleistocene humans (Atapuerca) had humanlike hyoids, unlike australopithecines, so modern human vocal tract anatomy was plausibly a derived feature of Homo, including Neandertals.

3. We have good evidence of pigment use from MSA Africa and Mousterian Europe. The Neandertals in particular appear to have been coloring skin with manganese crayons.

4. Decorative/ornamental artifacts were manufactured both by MSA Africans and Neandertals.

5. Neandertals shared the modern human-derived FoxP2 variant.

I have some notes on D'Errico's work (with Maria Soressi) on Neandertal pigment use that I'll post later. Given the confluence of the recent evidence from genetics, archaeology, and anatomy, I do not see how anyone can maintain the hypothesis that Neandertals (and presumably, other Late Pleistocene humans) did not have language.

Now, that is not to say that they (or any Late Pleistocene humans) were identical in their linguistic adaptations to living or recent people. I still think that communication is the most likely focus of evolutionary change in the Late Pleistocene -- but a change based within a pre-existing community of language users, not a newly-sprung linguistic skill. In fact, I think the next constructive step should be to characterize the variation in linguistic adaptations in recent people, who are surely not identical to each other. That verges on the subject of my presentation, which -- if you attend the AAPA meetings this spring, you will still get a chance to hear. That is, if you stick around until Saturday!

Yves Coppens and colleagues have found a frontal bone, and a bit more, in Mongolia. They do not report a date for the specimen beyond Late Pleistocene; it comes from a pit dug for gold mining. The site is north of Zhoukoudian and other northern Chinese sites by several hundred kilometers, and is approximately the same latitude (though further east) as Okladnikov Cave (discussed in my interview with Mica Glantz). The place is called Salkhit.

They describe the anatomy of the specimen: it has a complete supraorbital torus, thicker in the superciliary area than laterally; a slight frontal keel, and an overall sloping profile. In other words, it looks to be generally archaic in morphology. Their metrical comparisons put it generally with Middle Pleistocene crania like Zhoukoudian, Steinheim, and Petralona.

(via Paleoanthro)

References:

Coppens Y, Tseveendorj D, Demeter F, Turbat T, Giscard P-H. 2008. Discovery of an archaic Homo sapiens skullcap in Northeast Mongolia. Compte Rendus Palévol (in press) doi:10.1016/j.crpv.2007.12.004

Julien Riel-Salvatore reviews some reasons why kuru did not wipe out the Neandertals.

I don't have anything to add. The hypothesis comes from a paper in Medical Hypotheses by Simon Underdown; here's part of the abstract:

TSEs could have infected Neanderthal groups as a result of general cannibalistic activity and brain tissue consumption in particular. Further infection could then have taken place through continued cannibalistic activity or via shared used of infected stone tools. A modern human hunter-gatherer proxy has been developed and applied as a hypothetical model to the Neanderthals. This hypothesis suggests that the impact of TSEs on the Neanderthals could have been dramatic and have played a large part in contributing to the processes of Neanderthal extinction.

The short paper is admittedly speculative but quite clear. It does fail to cite the literature about selection on the prion gene, PRNP (I discussed it here in early 2006).

Riel-Salvatore points out all the reasons why it is probably wrong:

1. Neandertals were eating each other 100,000 years before they went away.

2. Neandertals didn't live as long as most humans who develop TSE symptoms.

3. Neandertals lived at much lower densities than the Kuru-spreading Fore people, and it's not credible for them to have spread a prion disease by cannibalism across this space (although, the urine-dispersed CWD seems to do spread pretty well through deer).

4. Non-Neandertals have a clear record of altering human skeletal remains also, including African Middle Pleistocene and early Upper Paleolithic Europeans.

I think these points are fatal to the hypothesis, unless we resort to a different mode of transmission; but in that case there is no reason to suppose that a prion disease would be involved rather than a viral or bacterial agent. I should also mention that despite early claims, there is not any reason now to think that the human prion gene was under long balancing selection.

References:

Underdown S. 2008. A potential role for Transmissible Spongiform Encephalopathies in Neanderthal extinction. Med Hypotheses (in press) doi:10.1016/j.mehy.2007.12.014

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

I've just been reading a useful paper by Andrew Millard, which reviews the chronometric dates of African and Near Eastern fossil hominids from the Middle and early Late Pleistocene. The overall theme is that we don't know the dates nearly as well as we would like -- or as well as many comparative analyses have assumed.

The highlight is the list of specimens with primary references to different date estimates. Anyone with a good training in paleoanthropology probably has a feel for which specimens have relatively good dates and which are real hands-up-in-the-air cases. Kabwe makes for a good example of the latter:

Kabwe (Broken Hill), Zambia. The remains of "Rhodesian Man," along with faunal remains, were discovered in 1921 by miners (Klein, 1973). The principal dating is based on Klein's (1973) assessment that the fauna is similar to that at Elandsfontein and broadly similar to those from Olduvai Gorge Upper Bed II through to Bed IV. There are no chronometric determinations. On the basis of the faunal correlation to Olduvai (Fig. 1), an age of younger than 1780 ka and, depending on the chronology for Olduvai, either older than 990 ka (on the long chronology) or, more likely, older than 490 ka (on the short chronology) may be assigned (see under Olduvai above). This is consistent with Elandsfontein being older than 330 ± 6 ka (Table 1).

Millard's discussion of "chronometric hygiene" takes up much of his discussion. This is nothing more than the simple idea that we should weed bad dates out of our analyses. For example, he singles out Florisbad as a specimen that has been handled poorly in the literature:

Use of the literature. In conducting this review of the chronometric evidence for African and Near Eastern hominids, the search for the detailed chronometric data was hampered by overreliance of many authors on the secondary literature. It is not uncommon to find a date cited from a publication, which upon checking simply cites another publication, which cites another, which cites the paper that first suggested the date. Frequently in such a chain of citations, the justification for the original date is lost, and in some cases, error limits disappear. For example, the ESR date of 259 ± 35 ka for the Florisbad hominid (Grün et al., 1996) can be applied to the Florisbad fauna, but somehow in the discussion of Stynder et al. (2001), this becomes simply "a maximum age of around 250 ka" (p. 372) for the Florisbad Faunal Span, and in McBrearty and Brooks (2000), it becomes a bald 260 ka age without any uncertainty for the Florisbad hominid itself. Sometimes, the primary proposal for a date is based solely on comparisons of morphology to the best-dated fossils at the time of publication, and for later papers to suggest evolutionary sequences based on this date is obviously problematic. Given the flux in dating methods, the fact that problems have often been identified some time after the introduction of these methods, and the changing understanding of the dates of faunal successions, every author should be beholden to check the basis of the dates cited and apply some basic chronometric hygiene (Millard 2008:19).

Of course, there is an irony here, since Millard's effort has generated a massive secondary source listing date estimates for all these hominids! I agree whole-heartedly with his sentiment, though -- everyone should do a better job of reading and citing papers.

But the effect of all this hygiene is to emphasize that most of the Middle Pleistocene remains a muddle, with very few well-resolved dates across the entire span. Millard describes faunal correlations as a relatively weak source of evidence in Africa. Above the time span effectively covered by ESR/TL, there is little to rely on.

References:

Millard AR. 2008. A critique of the chronometric evidence for hominid fossils: 1. Africa and the Near East 500-50 ka. J Hum Evol (in press) doi:10.1016/j.jhevol.2007.11.002

A flush of papers this week (two today in Nature, one tomorrow in Science) describe new analyses of SNPs across the genome. Two of the papers sample SNPs in global samples numbering more than 500 individuals.

This Reuters story by Maggie Fox is typical of the press coverage:

Gene studies confirm 'out of Africa' theories

WASHINGTON - Two big genetic studies confirm theories that modern humans evolved in Africa and then migrated through Europe and Asia to reach the Pacific and Americas.

...

The studies, published in the journal Nature on Wednesday, paint a picture of a population of humans migrating off the African continent, and then shrinking at some point because of unknown adversity.

Later populations grew and spread from this smaller genetic pool of founder ancestors -- a phenomenon known as a bottleneck.

These studies have very, very exciting potential. Here in my lab, we will be immediately using the data from these papers to test hypotheses about recent human evolution.

But it is beyond me to understand why anyone thinks that the "serial founder effect" story is news!

For one thing, the idea is based on 12-year-old research demonstrating that human diversity declines for some genetic loci with distance from Africa. This observation was replicated for genome-wide STR loci in a well-publicized paper three years ago. This paper clearly demonstrated how a model involving a chain of bottlenecks could result in a cline of diversity -- one population leaving Africa, a small group from this population moving to Jordan, another small group moving from Jordan to Mesopotamia, another small group from Mesopotamia to the Zagros, etc.

In other words, there's nothing new here. It's no surprise that genome-wide SNPs and copy-number variants (CNVs) should replicate the pattern already shown for genome-wide STRs.

What's worse, all these papers from the Stanford school of genetic orthodoxy fail to even test the hypothesis! I pointed out this problem three years ago:

The data that the paper attempts to explain are (1) the correlation of genetic distance and geographic distance among human populations, and (2) the decrease in genetic diversity in populations farther from Africa. We may ask, what other hypotheses would explain the same data? And what kind of evidence could test these hypotheses, instead of just asserting that they "match" the pattern of evidence.

One scenario that matches the evidence is multiregional evolution with a recent African dispersal of some adaptive genes. This is the hypothesis presented by Eswaran (2002). The idea is that human populations interacted for a long time in Africa and Eurasia, and that during the Late Pleistocene, adaptive changes within Africa allowed those populations to spread alleles into existing populations in Eurasia. The strength of the "founder effect" in this scenario depends on the genetic structure and selective advantage of the new African adaptive complex. Ramachandran et al (2005) actually cite Eswaran (2002) as an example of a serial founder effect. So the idea that there was widespread genetic movement out of Africa does not necessarily imply an out-of-Africa population replacement. The data do not require a replacement, and some -- even many -- of the genetic variants outside of Africa may have nothing to do with recent genetic movement out of Africa.

A second hypothesis is presented by Templeton (2002), who proposed that several founder effects happened at different times in the Pleistocene, each carrying one or more genetic variants out of Africa. The pattern of genetic variation appears to indicate that some genes left Africa during the Lower or Middle Pleistocene, while others dispersed later, during the Late Pleistocene. For Templeton (2002), this pattern indicates multiple dispersals, none of which was sufficient to wipe out the genetic contribution of earlier dispersals. This scenario also would lead to a pattern of correlation of genetic and geographic distance (because most genes have been affected by isolation-by-distance for a long time), while the recurrent dispersals would explain the decline in genetic variation outside of Africa.

A third hypothesis is that population size was simply greater within Africa than within Eurasia. The smaller population size (along with isolation-by-distance) would explain the difference in genetic variation; the correlation of genetic and geographic distance would be explained by isolation-by-distance. We may consider a fourth hypothesis also: that natural selection has tended to create slightly more genetic uniformity within Eurasia and slightly more genetic diversification in Africa. Such a scenario might be justified on ecological grounds: African populations cover a wider range of ecologies and have historically had a greater exposure to zoonotic disease, for example.

Except for the serial founder effect with population replacement, none of the other hypotheses are mutually exclusive. In other words, some genes might have been influenced by natural selection, most might have been somewhat influenced by differences in population size, but the largest effect might have been recurrent population dispersals.

Reading over the whole post, I think it did a good job of laying out the situation with serial founder effects in 2005, and there is little reason to change it now. Still nobody has tested the model! Again, this is a case of science by consistency -- the results of simulations generate the same kind of correlations as the observed data, so the authors claim support for their hypothesis.

But the necessary test should be carried out by dating haplotypes, finding the ages of "founder mutations" and eliminating the possibility of introgression from ancestral Eurasian populations. One of the key points in my earlier post is that the model proposed by Eswaran (2002) would generate exactly the distribution expected for serial founder effects -- despite the fact that it describes a wave of genetic change within an already-established pan-Old-World population.

This study doesn't support an out-of-Africa migration; it merely assumes it. Now, I'm one who thinks that there was an important trend of strong gene flow out of Africa in the Late Pleistocene. But data showing a correlation between diversity and distance from Africa just cannot show the critically important facts about the timing and magnitude of such gene flow.

Somebody will eventually straighten all this out. What I wonder is why it never seems to be the reviewers!

References:

Jakobsson M and 23 others. 2008. Genotype, haplotype and copy-number variation in worldwide human populations. Nature 451:998-1003. doi:10.1038/nature06742

Eswaran V, Harpending H, Rogers AR. 2005. Genomics refutes an exclusively African origin of humans. J Hum Evol 49:1-154.

Ramachandran S, Deshpande O, Roseman CC, Rosenberg NA, Feldman MW, Cavalli-Sforza LL. 2005. Support from the relationship of genetic and geographic distance in human populations for a serial founder effect originating in Africa. Proc Nat Acad Sci USA 102:15942-15947.

Templeton AR. 1998. Human races: a genetic and evolutionary perspective. Am Anthropol 100:632-650.

Templeton AR. 2002. Out of Africa again and again. Nature 416:45-51.