early modern

Earlier in the week, I pointed to a news story about upcoming research that substantiates some amount of gene flow among Pleistocene groups, persisting into living populations ("Multiregional evolution lives!"). That scenario made a bit of a splash in the news, but the result is not unprecedented.

Last year around this time, I noted a study by Wall, Lohmueller and Plagnol that came to a similar result -- estimating that around 5 percent of the gene pool of today's people outside Africa derived from ancestral non-Africans. That followed on earlier work by Plagnol and Wall from 2006 with essentially the same result.

Looking back at the blog, this has been a recurring topic since the beginning. For example, back in 2005 when I was still doing a meetings update, I posted about several conference presentations on the topic ("Genetics and multiregional evolution, meetings 2005"). At that time the new results were from Alan Rogers, Jody Hey, and Mike Hammer's lab, all suggesting that ancestral diversity either suggested some ancestral population structure outside Africa, or at least didn't reject it. A key finding was published by Garrigan and colleagues (2005), who found a pseudogene on the X chromosome with an unusually deep gene tree in East Asia ("Modern human origins: X marks the spot?").

But there's a lot of literature out there that contradicts this line of research. Some of it is still being published. A case in point is the paper released in PLoS ONE this week by Guillaume Laval and colleagues (2010). The key part of the abstract:

Our results support a model in which modern humans left Africa through a single major dispersal event occurring ~60,000 years ago, corresponding to a drastic reduction of ~5 times the effective population size of the ancestral African population of ~13,800 individuals. Subsequently, the ancestors of modern Europeans and East Asians diverged much later, ~22,500 years ago, from the population of ancestral migrants. This late diversification of Eurasians after the African exodus points to the occurrence of a long maturation phase in which the ancestral Eurasian population was not yet diversified.

That seems to directly contradict all the research suggesting some component of intermixture among pre-modern populations outside Africa. So what's the deal?

I have a good idea what's going on now with these apparent contradictions, thanks to a recent paper by Alan Templeton (2010). I'll discuss that paper in detail later this week, as I'm covering these issues now in my graduate seminar.

In the meantime, I want to give a little thought to the new paper by Laval and colleagues. Following through their simulation methods may give us some ideas about how we can resolve the discrepancies among these tests of human population history. I also want to explore some of the ways that paleontology and paleogenomics may help to inform our tests about these issues.

Here's a nice paragraph from the results section of the paper that outlines many of the simulation methods. I'd like to have seen some issues laid out more clearly, as some of the parameter combinations are hidden in the supplements and not clearly explained there. It means that as I discuss these, I may not quite have understood everything correctly.

First, we determined the evolutionary scenario that took place in the ancestral lineage that culminated in the emergence of modern humans (for a complete list of parameter symbols used along the manuscript, see Tables 2 and S4). We tested different evolutionary models [2], [5], [19], [22], [51]–[56] that allow different levels of introgression of archaic hominids to modern human populations. We assumed an early diffusion of archaic hominids (Homo erectus) out of Africa ~1.25 and ~2.25 million years ago [57], various ancestral migration rate intensities (m₀, ancestral migration rate is the proportion of migrants before the Out-of-Africa exodus) and an African exodus of modern humans between ~40,000–100,000 years ago [38]. By tuning the replacement rate δ, we then simulated scenarios that consider different levels of replacement of archaic hominids by modern humans (i.e. different levels of introgression of archaic material into the modern gene pool), including the most extreme cases of complete (δ = 1) and no replacement (δ = 0) as well as several scenarios with varying intermediate levels of replacement (Figures 3A and S2, Table S4). The summary statistics were calculated by merging all population samples (except for global F_ST) in order to minimize the effects of recent demographic events related to the continental populations. We thus considered in all models a constant size for the three modern human populations. The model with residual ancestral migration rate (m₀~10⁻¹⁰) and full replacement (δ = 1) clearly better fitted our data than any other model (Figure 3A, highest ψ1, the ψ1 of this model is significantly higher after correction for multiple testing when compared with the other ψ1 values, P<0.01). However, we could not discern between a complete (δ = 1) and an almost-complete (δ≥0.99) replacement of archaic hominids (difference between ψ1 is not significant for this pairwise comparison), indicating that a small contribution of archaic humans to our present-day genome cannot be completely ruled out [58]–[61].

For a long time, I've been bothered in the back of my mind about the outcomes of these analyses based on simulations and "approximate Bayesian computation" (ABC). I learned a long time ago never to argue statistics with a Bayesian. It's not that the approach is infallible, it's just that if someone is clever enough to use Bayesian statistics, it's going to turn into a long argument.

By my count the model has 18 parameters, and we could reshuffle them in lots of ways. Can it really be that no combination of the parameters provides a better fit than zero admixture? Intuitively, it seems wrong -- because it would mean that one combination of the other 17 parameters gave a near-perfect fit to the data. Perfect fits don't happen, not with genetic data as messy as in humans.

The conceptual scheme of the paper is an island model with migration, growth, and replacement as possibilities, between the three populations -- Africa, Europe and East Asia. Since any of the parameters could in concept vary from zero to infinity, each specific model ought to be a proper subset of the general island model, and they ought to grade continuously into each other. In other words, an out-of-Africa replacement is just one extreme of the general multiregional/admixture/introgression model.

That has some predictable consequences. A nonzero migration rate before a complete replacement ought to behave very much like a structured population within Africa before a replacement. An analysis that prefers the second really shouldn't be distinguishable from the first. Likewise, a very small population outside Africa before a slight replacement should look very much like a larger population with a more complete replacement. These options aren't identical, but they ought to grade continuously into each other.

But in the paper, the authors bounded the parameters in ways that make these different specific models discontinuous. For example, consider the parameter that defines the time of the initial population spread out of Africa:

We assumed an early diffusion of archaic hominids (Homo erectus) out of Africa ~1.25 and ~2.25 million years ago

If the time of founding of these populations could vary down toward the time of possible replacement (in the last 100,000 years), the continuity and replacement models would grade continuously. This would be the logical connection implied by the island model, but by limiting the range of times, the authors have generated an artificial difference between the models.

In principle, we could have a good reason for separating the models in this way. For example, we know that Europe and Asia were occupied by hominids before 1.25 million years ago, and we might specifically be interested in those people.

But in reality, we know that a 1.25-million-year old split between European and African populations is in conflict with paleogenomics. The Neandertal genome shows that we shared a small common ancestral population with Neandertal ancestors at most around 300,000 years ago, and possibly much more recently. If the human-Neandertal ancestral population was dispersed across Eurasia and Africa at that time, it must have had relatively high gene flow, enough so to behave as a single population with a small effective size.

So this is a possible problem. None of the "admixture" models included in the paper have a feature which the paleogenomic evidence says is necessary. My point is that the authors have generated a "rugged landscape" of models by eliminating the continuity between them. It may not be surprising that one choice of parameters fits the data much more strongly than alternatives, because the intermediates have not been examined.

There are other parameters for which uncertainty might be substantially reduced by using other evidence. For example, the authors consider a range of migration rates varying over three orders of magnitude between recent (modern) populations on different continents. The actual value of this rate has a large effect on the appearance of admixture, because it determines the likelihood that ancestral African variation has recently dispersed out of Africa into Eurasia. But we can probably obtain a good estimate of this rate of recent gene flow from other data, since we have large datasets of genome-wide SNP and microsatellite polymorphisms from these regions. These data could also provide a better test of the proposed Europe-Asia "split". Why are these aspects important? Because recent events will disturb or cover up the evidence for earlier dispersals and interactions. If we can constrain the recent events using other evidence, we can increase our power to test hypotheses about earlier events.

Although many possible intermediate models are excluded in the study, the authors in the end find an overlap in results between two apparently very different parameter combinations:

Among the 24 models tested, the model assuming a complete replacement rate of archaic hominids (δ = 1) and a residual ancestral migration (m₀~10⁻¹⁰) exhibited the significantly highest ψ1 except when compared with the model assuming an almost complete replacement rate of archaic hominids (δ≥0.99).

That result might seem paradoxical. At face value, it means that ancestral humans outside Africa did contribute genes to living populations, but only by means of very rare gene flow from Eurasia back into Africa before a subsequent replacement. In other words, the first modern humans in Africa would have been descendants of Africans and of Eurasian people. It's not surprising that the outcome is close to a model with very slight survival of Eurasian populations.

As we think of ways to improve these tests, I think we need to introduce independent tests of each parameter. This won't always be possible, and there will be cases where changing one parameter will impose a trade-off with one or more others. But that's the nature of these models -- each parameter is a dial, and twisting one of them may be corrected by turning others. The important point is that we can already falsify many of the conceivable possibilities. Until we have a model in which paleontology, archaeology, paleogenomics and the genetics of living people all form a single consistent picture, our work isn't done.

(see also, Gene Expression)

References:

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. 2005. Evidence for archaic Asian ancestry on the human X chromosome. Mol. Biol. Evol. 22:189-192. doi:10.1093/molbev/msi013

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

Laval G, Patin E, Barreiro LB, Quintana-Murci L (2010) Formulating a Historical and Demographic Model of Recent Human Evolution Based on Resequencing Data from Noncoding Regions. PLoS ONE 5(4): e10284. doi:10.1371/journal.pone.0010284

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

Templeton AR. 2010. Coherent and incoherent inference in phylogeography and human evolution. Proc Nat Acad Sci USA 107:6376-6381. doi:www.pnas.org/cgi/doi/10.1073/pnas.0910647107

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

I'm going to point to Rex Dalton's piece today with relatively little comment:

"Neanderthals may have interbred with humans"

Genetic data points to ancient liaisons between species.

The researchers arrived at that conclusion by studying genetic data from 1,983 individuals from 99 populations in Africa, Europe, Asia, Oceania and the Americas. Sarah Joyce, a doctoral student working with Long, analyzed 614 microsatellite positions, which are sections of the genome that can be used like fingerprints. She then created an evolutionary tree to explain the observed genetic variation in microsatellites. The best way to explain that variation was if there were two periods of interbreeding between humans and an archaic species, such as Homo neanderthalensis or H. heidelbergensis.

I understand that there is more to come on this subject in the not-too-distant future, and in this case I don't have anything on paper to go on. As everybody knows, I very much expected to find a similar result. Besides that, others have published similar outcomes based on resequencing data.

I titled the post, "Multiregional evolution lives," for a reason -- this study and others have been looking at genome-wide evidence of interbreeding outside of Africa. It's a multiregional model. Even I haven't been talking about levels of interaction as high as they are outlining in these models -- here they're looking at a genome-wide effect on neutral genetic loci, something you're not going to pick up significantly with today's samples unless it amounted to more than a couple percent of the human gene pool.

These ongoing studies are concluding that present-day genetic variation is inconsistent with a simple model where a random-mating ancestral population gives rise to today's global population by means of a staged out-of-Africa dispersal. They next look at a model with some substantial (possibly complete) isolation between ancient human populations followed by a subsequent out-of-Africa dispersal. They show that this model fits the data significantly better.

So far, so good.

For a moment, I'm going to adopt a critical perspective. Previous results haven't yet been able to answer an important possible question: Can they distinguish the effects of intermixture outside Africa from an ancient population structure inside Africa? Increasingly it looks like population structure inside Africa may have been very important to the evolution of Late Pleistocene Africans. How can we distinguish these kinds of structure from each other?

The short answer is that maybe we can't, yet. Human population history was not simple. If we take a simple model and add more parameters, it will fit the data better. The question is whether there may be some even better model with the same number of parameters. Population structure within Africa, selection on some loci but not others, asymmetrical migration -- all these and more might be possible.

I take it as very likely that the strict out-of-Africa replacement without interbreeding is no longer credible. We've moved beyond it, and all these papers are testaments to that. They're valuable.

But there's a lot of work left ahead of us, finding better models and continuing to test them with the increasing body of human (and ancient) genetic data. There's an awful lot up for grabs. Were Neandertals really a different species, a subspecies, or what? How genetically distinct were the groups within Africa that gave rise to the Middle Stone Age? Was there time for all recent humans to get Neandertal genes (as Jeff Long suggests in Dalton's story), or do some have a lot more than others?

As Dalton's story notes, soon we'll have the Neandertal genome, which will give an additional perspective on this issue from a point 40,000 years in the past -- like an eyewitness at the scene. This year, we'll begin to see whole-genome data applied to these questions. There may be other ancient genomes that will surprise us. And maybe those of us on the population genetics side still have a trick or two up our sleeves.

(Thanks to readers who forwarded this link!)

I got to sit down and watch most of the first episode of "The Human Spark" on PBS tonight (my earlier post). Our local station shows these things later than the national release dates, and I missed out on the first ten minutes or so as I was putting the kids to bed. The host is Alan Alda, and here are my live-blogging thoughts after I sat down to watch:

8:16: Svante Pääbo interview. Alda watches Adrian Briggs drilling into ancient bones. Explains the problems with contamination.

"But that small difference between us could be crucial, couldn't it?"

8:18: Now, on to protein extraction from Neandertal bones to do isotopic analysis. Alda sits down in the cafeteria with Michael Richards, explaining the high proportion of animal protein in the Neandertal diet.

8:19: On to Grenoble. Nice shot from an Alp. The European synchotron. Tanya Smith is here beaming X-rays into them to get micro-CT data from inside the teeth. The skull here is from Roc de Marsal.

Some interesting animations of human versus chimpanzee cranial growth. Human brains develop slowly, etc.

"Neandertal children ... seem to have grown up more quickly..."

We're in the archaeological site of Roc de Marsal, with Harold Dibble and Shannon McPherron. How many Neandertals were there at any one time. They banter about 20,000, decide that's too many.

8:23: Dan Lieberman is showing Alda the original Skhul 5 skull. We've got a graphic of modern humans evolving in Africa, like little campfires from a night view of the Earth. And then they spread out to light little campfires in Europe. It's like the George Bush version of human evolution -- "a thousand points of light!"

Close shots of archaeological levels with Randall White.

8:27: "Even if Grandma kept her teeth in a glass..." Pierced human molars, being worn as ornaments. They go through the little museum near the site. "Microscopic analysis that we've been doing shows that they were sewn on, like to articles of clothing." This is a nice conversation they're having.

It's a little unfortunate that the film pushes the "no Neandertal ornaments" angle, particularly since this week's paper with the pierced shells.

"Here's what I don't get: The Neandertals survived, but didn't change. They came from the same people that we came from, and at some point we started changing; we became able to change.... Having come from the same background, why were we able to change and they weren't?"

White's answer -- Neandertals have a generalized technological approach; modern humans invent new technologies to address every problem that comes along. You can't separate society from technology (as a response to a followup about social organization). Population numbers may have limited lines of communication among Neandertals. With moderns, "once somebody invents something, everybody knows about it."

8:35: John Shea is teaching undergraduates how to knap. Explaining the value of projectile technology. Ooooh -- time to hit a deer decoy with an atlatl dart. "A hunter who's using this kind of thing would have to work with a group...it takes planning, cooperation...I can't imagine this functioning without the prior existence of language."

I find myself thinking wondering why this wouldn't have been true of Neandertals hunting the same animals? And didn't we hear a little while ago that it was the small animals and fish that set modern humans apart? There is a problem with the presentation here -- these seem contradictory.

8:40: Now, we're in Nairobi with Veronica Waweru. Looking at arrows with reusable shafts. Alda is narrating -- did modern humans start using poison?

8:43: Olorgesailie. Alison Brooks and (an unnamed) Rick Potts are there. Brooks has points that are 150,000 years old that may be arrow points (although the one they handle on camera is bigger than Shea's atlatl point...). Three different excavations, each representing a different age. Another small point "has just been unearthed". This one looks a likelier arrow point than the other. Then, 320,000 years old, they have left a bunch of small stone flakes on pedestals for the film crew. The stone raw material is taken from at least 45 to 50 km distance. Alda: "These people were choosy about their materials...quite unlike the Neandertals."

This is unfortunate, too -- there are some clear instances of Neandertals transporting raw materials over 250 km.

Now they're looking at a possible anthropogenic accumulation of pigment minerals. Brooks stresses human "inventiveness" as a cause of the success of modern humans.

8:50: Back to Ian Tattersall. I didn't see his earlier appearance. "When did people who would fit into human society now first appear?" Tattersall puts it down to 50,000 years ago or so. He suggests that the biological ability to behave in modern society might date back to 150,000 years ago, but lay latent until culture developed much later to bring out the modernity.

Whoa -- the points of light again. People are swarming like tiny sparking ants, and all the yellowish Neandertal fires are going out.

Not a bad program. Alda was a great host for this. You can tell he's genuinely interested in this stuff, and he really put the scientists at ease in the interviews. It's great that they got usable material again and again just having him talking with the archaeologists. And having one host actually travel to these field sites was great -- much better than the usual disembodied narration.

I was really liking it until around halfway through, but as the film went on, it started to raise contradictions that bothered me. Very one-sided about Neandertal behavior, too simplistic.

I don't think the interviewees were the problem here, I think in particular Shea and White were making fairly nuanced statements about Neandertals. I can guess that if either had given any black-and-white quotes, the editors would have included them. My impression was that the choice of topics dictated the result -- ornaments, pigment, and projectiles were chosen to emphasize the "behavioral modernity".

Where I think that approach fails in in the specifics. Projectiles may have been technically more difficult than large-point weapons, but they should have been socially easier. Does it take less cooperation to bring down large animals with close-contact weapons? I think it's the opposite -- I think Neandertals must have been under more pressure to cooperate in their hunts. The transport across long distances is important in MSA contexts, but it's also present in Mousterian France. Neandertals didn't spend hours and hours making beads, but they did wear ornaments and use pigments. If there's a distinction, it's the frequency of these behaviors -- which is a lot harder to measure or estimate.

It's too bad in a way -- it really wasn't necessary to talk about the "human spark" as a human versus Neandertal comparison. This didn't have to be a "modern human origins" program. The DNA segment was interesting, but it didn't really contribute anything to the show's theme -- the narration concluded the segment by saying that the genes don't tell us about the "spark" yet.

I'd have emphasized some older stuff, which is new science that actually does tell us about the emergence of humanness. The Brooks segment would fit into that theme, with the much earlier material from Olorgesailie (and this week we have 500,000-year-old blades from the Kapthurin Formation...). I'd have emphasized the new stuff from Atapuerca, especially the evidence about language. An earlier focus would bring a little more credible use of genetics, either FOXP2 (which I really don't need to see again...) or some human-accelerated genes.

It's curious to compare this program with the NOVA series last fall. The themes were very different (NOVA emphasized climate, this one technology). There was very little overlap of scientist lists -- although it never hurts to be based in New York. I think the programs go well with each other, but it sort of forces the casual viewer to notice that the same evidence can be read almost at cross-purposes, depending on what the scientist assumes is fundamental.

Debbie Guatelli-Steinberg and Donald Reid report on the perikymata spacing of a sample of fourteen anterior teeth from Qafzeh. These are "early modern humans", among the earliest to be located outside of Africa, but their anatomical position relative to Neandertals and other groups has been subject to frequent dispute.

As I've emphasized several times ("Neandertal teeth: the other shoe", "How modern is "modern tooth development"?"), this growth characteristic of teeth is variable among living human populations. What remains totally unclear is why it varies.

Neandertals are at the low end of the human range of variation for perikymata counts on their anterior teeth, and the patterning of packing across the tooth is somewhat different. In particular, Neandertals have fewer perikymata nearer the roots of these teeth (for details, I suggest Guatelli-Steinberg's 2009 review article).

The current paper follows up on earlier work by Janet Monge and colleagues (2006). They emphasized that the Qafzeh anterior teeth fit within the overall human range of variation, but observed that two individuals were very close to Neandertals in their packing patterns. Here, Guatelli-Steinberg and Reid include more specimens in the sample, confirming this similarity.

From their conclusion:

The purpose of this study was to investigate whether Qafzeh teeth are different from those of modern humans in the percentage of perikymata present in their cervical [sic] appear to fall in the lower 50% of the modern human distribution, and a few fall within the lowest 5% of the distribution. Thus, this sample of Qafzeh teeth appears to differ from those of modern humans in the same direction that Neandertals do: with generally lower percentages of perikymata in their cervical regions. As can be seen in the SEM montages in Figure 2, perikymata become much more closely spaced in the cervical relative to incisal halves of the Inupiaq LI2 than they do in either the Neandertal or Qafzeh LI2s. Although sample sizes precluded a similar test between the Qafzeh and Neandertal teeth, plots of the averages for these teeth (Fig. 1a,b) reveal the similarity of the Qafzeh and Neandertal teeth, particularly for the UI2, LC, LI2, and LC. Values for two of the Qafzeh UI1s and a single UC are closer to the modern human than Neandertal means for these tooth types, revealing overlap in the ranges of values, as is also true for Neandertals and modern humans (Guatelli-Steinberg et al., 2007).

It may be worth pointing out that the perikymata packing pattern was a key part of Ramirez-Rossi and colleagues' conclusion that the Les Rois B mandible as well as several other Les Rois dental specimens show affinities to Neandertals.

I think Monge and colleagues are correct in asserting that this packing pattern is not a taxonomic diagnosis. Notwithstanding that the precise Neandertal-like pattern, present at Qafzeh, does not occur in the known human samples, we still don't know why human patterns differ from each other. In their discussion, Guatelli-Steinberg and Reid suggest alternatives for the mechanism forming the straiae, but I'd like to have some kind of genetic answer -- what developmental processes changed, carrying this feature along with them?

Anyway, another contrary observation to the idea of "modern human dental development", I guess.

References:

Guatelli-Steinberg D, Reid DJ. 2010. Distribution of Perikymata
on Qafzeh Anterior Teeth. Am J Phys Anthropol (in press). doi:10.1002/ajpa.21158

Guatelli-Steinberg D, Reid DJ, Bishop TA, Larsen CS. 2005. Anterior tooth growth periods in Neandertals were comparable to those of modern humans. Proc Nat Acad Sci USA 102:14197-14202. doi:10.1073/pnas.0503108102

Guatelli-Steinberg D. 2009. Recent studies of dental development in Neandertals: Implications for Neandertal life histories. Evol Anthropol 18:9-20. doi:10.1002/evan.20190

Monge JM, Tillier A-M, Mann AE. 2006. Perikymata number and spacing on early modern human teeth : Evidence from Qafzeh cave, Israel. Bull Mem Soc Anthropol Paris 18:25-33.

Ramirez Rozzi FV, d'Errico F, Vanhaeren M, Grootes PM, Kerautret B, Dujardin V. 2009. Cutmarked human remains bearing Neandertal features and modern human remains associated with the Aurignacian at Les Rois. J Anthropol Sci 87:153-185.

Science journalist Richard Stone writes in the current Science about new Late Pleistocene skeletal remains from Guangxi: "Signs of Early Homo sapiens in China?"

The big prize is the Homo mandible, whose owner would have had a chin that curved ever-so-slightly outward. H. erectus had an inward-sloping chin, whereas modern human chins generally jut out farther than the Guangxi specimen's. Jin's group classifies the fossil as primitive H. sapiens and says the intermediate chin suggests interbreeding with H. erectus. Uranium isotope dating by R. Lawrence Edwards of the University of Minnesota, Twin Cities, indicates that the fossil-bearing layer is about 110,000 years old, in a paper that will appear in the November issue of Chinese Science Bulletin.

The article frames the discovery as a challenge to the "Out of Africa" hypothesis of modern human origins, thereby giving the "out of Africa" defenders several chances to rebut. That framing comes from the discoverers, who are pushing the "early modern" aspects of the jaw.

I don't think the modern/nonmodern classification is very productive. Here's a mandible with a chin -- a small chin, but apparently a real mental trigone (the article is accompanied by a photo, not the greatest). It's no less "modern"-looking than most of the 100,000-year-old Klasies River Mouth mandibles (thanks to a reader for noting that one). Some Neandertals had chins, and some much earlier humans came pretty darned close. A chin is not a diagnosis, it's a symptom.

Here's a better question: what explains the epidemic? The same anatomical feature, showing up in widespread geographic locations within the past 100,000 years? If these populations were isolated with no gene flow between them, the chin must have appeared coincidentally by convergent evolution. The other alternative is that these ancient human populations traded some genes.

How unlikely is the chin, really? Is it a developmental side effect of a single genetic change? Would that make it more likely, because no combination of factors is required? Or less likely, because a single mutation causing such a strange effect would be very improbable to begin with?

References:

Stone R. 2009. Signs of Early Homo sapiens in China? Science 326:655. doi:10.1126/science.326_655a

On occasion, I point out interesting findings from archaeological chemistry and microscopic study of site formation processes. Last month, I pointed to the ability to distinguish animal and plant fat residues on ancient artifacts. Before that, there was the discovery of flax fibers from the Upper Paleolithic of Dzudzuana Cave, Georgia.

In July, a paper by Paul Goldberg and colleagues described the "micromorphology" of the sediments from Middle Stone Age levels of Sibudu Cave, South Africa. The excavations at Sibudu have been able to distinguish many distinct stratigraphic units with distinctive spatial locations and compositions. Micromorphology involves looking at these sediments in microscopic detail, picking out small grains of crushed bone, charcoal, plant fibers, phytoliths, and other materials.

Goldberg and his colleagues were able to make some very cool observations. For one thing, they have charred drips of broiled grease:

Two types of amorphous organic combustion remains were identified in samples from Sibudu: a type with a typically vesicular texture and a type with a cracked texture. The first type was found as isolated bodies, subrounded with a diameter of 10 µm to 1 mm, and they exhibited no evidence of cell structure. Bubbles or vesicles give the bodies a highly porous nature, and they are often thin walled. The microstructure of these homogenous or finely heterogeneous isotropic particles and their droplet-shaped occurrence suggest that these bodies were originally fluid and that they underwent a degassing process but have since hardened. These bodies resemble char and are probably derived from the burning of flesh or animal fat (104-105).

Mmmmm...MSA barbecue. The other type of "amorphous organic combustion remains" are charred resins, from trees or seeds. Mmmm...MSA smokehouse.

Second, they have beds.

Because of its long fibrous nature, it seems that this material consists of herbaceous plants, possibly some type of sedge, reed, or grass. There is no evidence to suggest that this plant would have grown naturally in the rock shelter, and the presence of clay aggregates derived from the river valley found in association with the laminated plant fibers implies that the grass or reed was transported to the cave from the nearby Tongati River by the shelter’s inhabitants.

The compact and laminated structure of the organic fibers in this microfacies also suggests that, once brought to the cave, the grass or reed was subjected to compaction, most likely through trampling. Further evidence supporting the interpretation of trampling is seen in the stringers of charcoal, clay aggregates, and burnt bone that define horizontal and subhorizontal surfaces on top of and within the laminated organic fibrous material. Pieces of éboulis and lithic fragments also define surfaces wi thin the microfacies. The fact that this grass or reed was transported to the cave by humans and that once there it was influenced by human trampling suggests that this microfacies represents a type of constructed bedding. If this is the case, then Sibudu contains the oldest evidence for constructed bedding, significantly older than that reported at the open-air site of Ohalo in Israel (Nadel et al. 2004).

The bedding material was in some instances burned, in some instances swept or trampled in such a way that the regular alignment of the phytoliths was jumbled and disrupted. They interpret this as efforts to "maintain" the site -- in other words, housekeeping:

What seems a likely and reasonable scenario is that the original organic matter of this laminated layer of sedges, grass, or reeds was completely combusted, resulting in total ashing of the organic material. The calcitic ash in this microfacies was transformed through phosphatization, as evidenced by the presence of a few remnant pockets of phosphate in this microfacies. The fact that large crystals of gypsum often form directly below these phytolith layers provides suggestive evidence for the downward leaching of CO₃- or P-rich solutions.

Just an aside -- that is such interesting chemistry, like the organic materials and ash are melting down into the underlying deposits.

The association between microfacies 2 and 4 suggests that the sedges, grass, or reeds that were brought into the cave for bedding were usually burned and probably by humans when they no longer used the bedding. This observation explains the sequence seen in samples SS-6 and SS-5 of laminated nonburnt fibrous organic material grading into laminated burnt fibrous organic material with phytoliths (microfacies laminated type 2B); the sequence is finally capped by a layer of laminated phytoliths.

Why did they burn the stuff? The authors guess that they were trying to cut down on parasites:

Together, this evidence shows that not only were the occupants of Sibudu bringing grass or reeds into the cave—likely for the construction of bedding—but they were periodically burning them, possibly as a means to remove pests or insects that had colonized the beds. (Smoldering goat dung and organic matter can be observed in many parts of the Middle East, including Hayonim, where tick removal is one of the important objectives; P. Goldberg 1992, personal observation.)

The MSA at Sibudu dates to between 45,000 and 65,000 years ago, with the best evidence for bedding in the units that OSL puts around 50,000 years ago. The implications of the "site maintenance" and spatial characteristics of the site are mentioned in the paper's conclusion:

Organization of living space, and particularly a deliberate use of space, has been suggested by Wadley (2001) and also Binford (1996) as an important trait of culturally modern behavior, reflecting a more complex social organization. While the evidence from the laminated units at Sibudu may reflect such organization, the lack of evidence for such spatial organization, such as is the case for the lower homogeneous layers at Sibudu, should not automatically suggest that occupation in these units was any less complex.

If spatial organization of living space is a "modern" behavioral feature, it is one shared by Neandertals (I noted that briefly in a 2006 post). But then, it's shared by any number of invertebrates, also. I think the interpretation of this kind of behavior will have to wait until we have more sites investigated with comparable methods. As the introduction to the current paper points out, a lot of spatial information could be brought out of these micro-scale studies, if they were conducted routinely.

References:

Goldberg P, Miller CE, Schiegl S, Ligouis B, Berna F, Conard NJ, Wadley L. 2009. Bedding, hearths, and site maintenance in the Middle Stone Age of Sibudu Cave, KwaZulu-Natal, South Africa. Archaeol Anthropol Sci 1:95-122. doi:10.1007/s12520-009-0008-1

I'm a big booster of the idea that human demographic expansion helped drive our recent evolution. So you might expect me to like the new paper by Adam Powell, Stephen Shennan and Mark Thomas, titled, "Late Pleistocene demography and the appearance of modern human behavior." Yet, I see a lot of weaknesses in the paper. I think the paper tries to sidestep several issues about "modern human behavior" that ought to be tackled head-on. In the end, the model in the paper can't describe the data the authors want to consider. Maybe they should have adopted a different model; maybe different data.

I've taken a lot of notes about this -- too many for me to share, but I wanted to review the basic exposition of the paper, including why the authors think demography may determine technological change during the Late Pleistocene. I might post other notes later on the issue of genetic modeling of demography and its relevance for archaeology.

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

References:

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

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

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

I can understand that National Geographic wants to promote news from researchers who take National Geographic money. It's only natural, and as a publicity organ for paleoanthropology, they haven't done so badly in the past.

But this story titled, "Humans 80,000 Years Older Than Previously Thought?" is just silly.

Giant clams are in the news today, helping to drive the expansion of modern humans out of Africa. Can we believe it?

• The paper (Richter et al., 2008) describes a new species of giant clam, distinct from others in reproductive cycle, habitat preference and size.
• This new species is mainly found in shallow water reefs.
• Today, the species makes up a very small proportion of the total Red Sea giant clam count.
• Before the last interglacial, this species made up as much as 80 percent of the giant clam count, as assessed by shells from reef terraces. This proportion decreased around the last interglacial, and again in historic times.

This sounds like the classic megafaunal exploitation story, as it is being reported. Shells become an important debris of humans in Northeastern Africa by 125,000 years ago (Walter et al., 2000), and were important elements of the MSA along the coasts of North and South Africa (McBrearty and Brooks, 2000). So it would not be surprising if these people recovered giant clams, particularly if those clams were readily available in shallow water. Giant clams are similar to large tortoises in terms of their recovery and exploitation, and there is already good evidence that tortoise size decreased with overhunting as Late Pleistocene human populations grew. By the Upper Paleolithic, people in some parts of the Mediterranean began to harvest small shellfish to an extent that put pressure on their populations. The giant clams would be an early example of the same phenomenon, made more precarious by the shallow-water habits of this particular clam species.

Since refuting the Neandertal inferiority complex is a theme this week, I should point out that Neandertals who lived on the coast also exploited shellfish, an observation that I discussed here. The exploitation of coastal resources is not specifically“modern”. Coastal populations of terrestrial predators typically eat marine species, for example, coastal brown bears in Alaska systematically harvest soft-shelled and razor clams (Smith and Partridge, 2004).

So the clams shouldn’t be surprising. Are they interesting? I think it is another piece of evidence that human populations in Africa during the last interglacial were already large and growing. Archaeological sites from the African Late Pleistocene have been proliferating during the last few decades, but are still underrepresented compared to the density of sites in other regions, especially Europe and the Near East. So you might not get the idea from archaeological sites that the African population was especially large. Yet, across the MSA, we see increasing breadth of faunal exploitation and some systematic recovery of small resources such as shellfish and tortoises. We also see a greater intensity of raw material exploitation and movement, and

Most important, we now have clear genetic evidence for a large and diverse African population during the Late Pleistocene. That includes the mtDNA genealogy, which now supports the interpretation of an effective population size that had perhaps doubled or more by the last interglacial (I discussed that research here). Put that together with the evidence for structure within this ancient population — either regional differentiation or ecological adaptation — and we have some very interesting demographic knowledge about Africa 100,000 years ago.

References