Late Pleistocene

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

Exponential growth is a feature of current human populations, and was may represent how the human population behaved during some episodes of its demographic history. However, "exponential" can mean different things to different people, if you're not used to thinking mathematically about growth. So I need to lay out some definitions:

That was the headline of many of last week's stories about the paper by Behar and colleagues, drawing upon the Genographic Project African mitochondrial DNA (mtDNA) data. Here's a quote from the National Geographic Society's press release:

Previous studies have shown that while human populations had been quite small prior to the Late Stone Age, perhaps numbering fewer than 2,000 around 70,000 years ago, the expansion after this time led to the occupation of many previously uninhabited areas, including the world beyond Africa.

And here's project director Spencer Wells' quote in the same release:

Dr. Spencer Wells, National Geographic Explorer-in-Residence and Director of the Genographic Project, said: "This new study released today illustrates the extraordinary power of genetics to reveal insights into some of the key events in our species' history. Tiny bands of early humans, forced apart by harsh environmental conditions, coming back from the brink to reunite and populate the world. Truly an epic drama, written in our DNA."

Well, that certainly sounds dramatic. But is it true?

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

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.

Charles Q. Choi reports on a new paper by Michael Richards and colleagues:

For the past 30 years, studies of their skulls, jaws and teeth suggested cave bears might have been largely herbivorous. In addition, the bones of central and western European cave bears matched those of vegetarians in having low levels of nitrogen-15, whose atomic nucleus has one more neutron than common nitrogen-14 does. Animals accumulate nitrogen-15 in their bodies, and animals that eat animals -- that is, carnivores -- build up more nitrogen-15 than herbivores do.

Still, black bears and brown bears are omnivores. This suggested that although some cave bears were largely vegetarian, others might have been more carnivorous.

New data from the Pestera cu Oase ("Cave with Bones") in the southwestern tip of the Carpathian mountains in Romania now hints most of its cave bears were significantly carnivorous, due to their high nitrogen-15 levels.

It's PNAS, so we won't see the paper for a while. I'll comment more fully here when it is available. Nitrogen-15 is the primary evidence for Neandertal carnivory also, although as I've noted (here and here), those interpretations face some complications.

A large source of nitrogen-15 is fish, which seems a likely source for the cave bears.

UPDATE (2008/01/08): I got the paper. The results show that the Oase cave bears have nitrogen-15 values ranging from a low overlapping with red deer up to a high midway through the wolves -- where higher means more carnivorous. There was one outlier with a very low nitrogen-15 ratio. The impressive thing is the range of values, which apparently exceeds the ranges in other species.

In comparison with other European cave bear samples, the Oase specimens are not alone in showing evidence of carnivory, but the vast majority of specimens from other sites (n=105) have values in the red deer range or lower.

Axes of variation

The paper suggests that the high nitrogen-15 in the Oase cave bears could not have come from the local ungulates (red deer and ibex) because their carbon-13 ratios are extremely different from those species. I think that's a fair speculation, but really there are too many dietary parameters to get an estimate from these two ratios. For example, a primarily vegetarian diet that included a significant amount of fish might explain both ratios (and the wide variation in nitrogen-15, since bears compete for fishing access).

But there are other possible axes of variation. Life history and behavioral variation can affect the isotope ratios. Some of the cave bears across Europe have very low (lower than ungulate) nitrogen-15 values. Hibernation has been suggested previously to explain the correlation of nitrogen-15 values with estimates of temperature, the idea being that bears facing colder winters are dormant for longer periods.

The hibernation story raises the question of the impact of long-term climate change on isotope ratios. The channel through which climate changes may affect the uptake of different isotopes into plants and animals is unclear -- it seems to involve temperature and rainfall as they modulate diet availability. Here's a chart of the carbon and nitrogen stable isotopes in Pleistocene Europe in three different carnivores:

Carbon (top) and nitrogen (bottom) stable isotopes in European herbivores (horse, cattle, and deer) over time. Figure 1 from Hedges et al. 2004.

None of this casts any doubt on the paper's results -- the Oase cave bears simply seem to have been higher on the food chain than most other cave bears sampled across Europe. I just raise them to note the demands that paleoecologists are placing on these isotope ratios. Especially when the species in question has substantial dietary flexibility, like bears, we should probably figure that diet choices are the largest component of variation. That means that we should probably be skeptical about the impact of smaller-scale variations, such as climate, unless there is very strong evidence for dietary stability over the relevant time scales.

Since many large European mammals were undergoing large range contractions or extinctions during this time period, we should expect that the surviving species may have undergone substantial changes in niche partitioning and dietary choices. Humans -- whose isotope ratios are in many ways the most interesting -- would be included in this number.

Bear paleoecology

I think the best passage from the paper is the end of the discussion, where the authors compare the dietary and ecological flexibility of extant ursids as a way of contextualizing the cave bears.

As a consequence of these ₁₅N values, the dietary ecology of modern, higher-latitude bears (excluding polar bears) is relevant for that of cave bears, especially the North American brown bears (U. arctos, including the Kodiak and grizzly bears) given their high-latitude range, body-size variation, occupation of regions with less human ecological impact than most of Eurasia, and extensive database. Brown bear diets range from almost completely vegetarian, including ones with substantial amounts of fruit/berries, to ones containing a substantial amount of fish and/or ungulate meat (19-21, 29, 30, 44, 45). All aspects of their omnivorous diets have limitations in availability, potential feeding rates, and nutritional value in any given environment; adequate weight gain for survival, reproduction, and hibernation therefore depends on a mix of as many food resources as are available (19, 21). Meat consumption, in particular, varies widely among and within brown bear populations, due, among non-maritime bears, to the availability of ungulate fauna (29, 30, 44, 45). Large adult males also appear to be more carnivorous than females or subadult bears (28, 29). North American black bears (U. americanus) appear to have similar plant/meat dietary proportions as brown bears (29), except that the larger brown bears are frequently more carnivorous when the prime meat is maritime (e.g., salmon) (46). This ecological flexibility of modern brown bears therefore makes an appropriate model to understand the range of isotopic values now available for European cave bears, both within and between site-specific samples (Richards et al. 2008:4).

Europe presents a problem of bear competition similar in many ways to the current North American case, in that different ecologically flexible species are differentiated by size. In North America, the larger brown bears exclude access to salmon fishing sites from the smaller black bears.

But in Europe, the brown bears were the smaller species. That helps to make sense of the isotope results on Pleistocene European brown bears, which have even lower nitrogen-15 values than the cave bears (Bocherens et al. 2004).

As for the cave bears, I suppose not even pic-a-nic baskets are out of the question....

A genetic afterthought

There is also this:

Genetic Affinities. To provide additional confirmation of the morphological evidence, mitochondrial DNA (mtDNA) was extracted, amplified, and sequenced from 19 ursid samples (SI Table 2). All 19 individual sequences of the Peçstera cu Oase ursids show clear affinity to central European cave bear sequences (35) rather than to brown bears. They do not form a monophyletic group within cave bear mtDNA variation, and the range of the Oase bear haplotypes is spread throughout most of the variability known for central European cave bear populations from southern Germany, Austria, Croatia, and Slovakia (35-37).

If we expect to have any hope of working out the phylogeography of ancient humans (like Neandertals), then we have to be able to work out the movements of many ancient mammals. That's the only chance of cross-The cave bears look a bit like the Neandertal pattern -- probably not surprising since they are both medium-bodied omnivorous mammals. That's encouraging.

References:

Bocherens H, Argant A, Argant J, Billiou D, Crégut-Bonnoure E, Donat-Ayache B, Philippe M, Thinon M. 2004. Diet reconstruction of ancient brown bears (Ursus arctos) from Mont Ventoux (France) using bone collagen stable isotope biogeochemistry (¹³C, ¹⁵N). Can J Zool 82:576-586.

Hedges REM, Stevens RE, Richards MP. 2004. Bone as a stable isotope archive for local climatic information. Quatern Sci Rev 23:959-965. doi:doi:10.1016/j.quascirev.2003.06.022

Richards MP, Pacher M, Stiller M, Quilès J, Hofreiter M, Constantin S, Zilhão J, Trinkaus E. 2008. Isotopic evidence for omnivory among European cave bears: Late Pleistocene Ursus spelaeus from the Peçstera cu Oase, Romania. Proc Nat Acad Sci USA (online early) doi:10.1073/pnas.0711063105

I've had a very busy couple of days, and haven't been maintaining my reading-and-linking as much as I had hoped. So I wanted to take a few minutes to do a quick tour of the blogosphere to see what people are saying about the idea of acceleration.

I'm linking to posts I have read, and in some cases commented on. They are a mix of explanation of the concepts, applauding the ideas and analysis, and criticism of the methods. What I most want to point out is that the discussion on blogs is at a very high level -- people are reading the paper with much more precision than I have ever experienced in the peer review process. This is really the best that today's science community has to offer.

One of the best posts is over at LiveJournal, where shoshin works through the theoretical part of the paper. Naturally, this is my favorite part -- and shoshin describes things exceptionally well. The beginning is great:

The case for a recent acceleration of human evolution in the last 40K years (and especially the last 10K) follows pretty straightforwardly from evolutionary first principles combined with elementary facts about human history since the late Pleistocene. So straightforwardly, in fact, that you have to wonder why nobody thought of it sooner. It's one of those rare cases where the theoretical argument is so strong that you can pretty much use accordance with it as a test of experimental methods at least as much as the other way around.

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Razib works through the paper at Gene Expression, in a long, detailed post. I like this part:

We are now the most numerous large mammal on the face of this planet. Using the data above the authors imply that our species has been subject to somewhat more that 1/2 a substitution per year. Remember, a substitution is a replacement of one allele for another at a locus on a population wide scale. If this is correct that means right now every few years alleles driven by selection are being fixed within our species.

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At the old-school Gene Expression, p-ter posts some analysis and critiques. A great comments section has arisen on this post, including comments from some of the principals, and general comments about the quality of the discussion on blogs compared to the journal process. I've answered some of the points in my rarely asked questions post, but the most powerful part bears repeating:

Every distribution has a tail, so if they were to move their threshold a bit further to the right, surely they'd be able to narrow down the number of regions to something consistent with a constant rate. That is, the entire argument is predicated on perfectly identifying selection in the regions of the parameter space they search. This is a major assumption, and not one I'm willing to make without strong evidence. They provide none.

Actually, with an acceleration of around two orders of magnitude, we can tolerate a lot of slop in the estimates. We don't need to perfectly identify selection -- in fact, we'd still have strong support for rapid acceleration if we threw away 95 percent of our data! Naturally, we don't have to do that -- our methods are based on a threshold that eliminates nearly all false positives, and we are missing the vast majority of events. For one thing, the LDD test doesn't find selection on multiple alleles at the same locus. I am working on new methods that will find some of these kinds of events, but for the time being we continue to interpret all things conservatively.

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Andrew Sullivan posts approvingly:

I posted on this potentially world-changing research this afternoon. Here's a helpful, chatty, specialist blog with lots of extra links if you're scientifically literate and curious.

What I want to know is, sure, Razib is helpful and chatty, but what am I, chopped liver?

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Larry Moran has added several posts on the research, starting with this one:

In addition to the major flaw in logic, there are many other things wrong with the claim that modern humans have stopped evolving. The claim carries with it a very loaded assumption that is never explicitly stated. The assumption is that humans have pretty much reached their optimal level of fitness for all other characteristics. For example, we are no longer selecting for higher intelligence, or a better immune system, or more efficient energy production, or stronger muscles, or any of a host of other things that might make us better adapted to all environments.

Why is this assumption necessary? Because nobody could possibly suggest that we have stopped evolving without assuming that we have reached optimal fitness for all those things in our present environment.

Larry follows with several other posts, some critical, focused in part on the problem of how much evolution is explained by positive selection as opposed to other forces.

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Nature's blog, "The Great Beyond" notes the paper and the resulting discussion.

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More will follow...

n. b. This is a story about my work on recent human evolution, describing some of the main results and how the work came about. The story refers to my paper (with Gregory Cochran, Eric Wang, Henry Harpending, and Robert Moyzis), "Recent acceleration of human adaptive evolution," which came out in December, 2007.

Like most good stories in biology, this one begins with Darwin. Darwin was always very interested in animal breeding, which he considered the best analogy for the process of natural selection. Of course, if you're breeding livestock and want to select for some characteristics, it is important to select from as large a herd as possible, because large populations have more variation in them. Darwin recognized this as an important condition for natural selection, which relies on sufficient variation in natural populations.

[A]s variations manifestly useful or pleasing to man appear only occasionally, the chance of their appearance will be much increased by a large number of individuals being kept.... Hence, number is of the highest importance for success.

These words from the Origin, "number is of the highest importance for success" were influential.

This is a quick review of the research, based on a presentation I gave earlier this year. It is not complete, and glosses a number of very important details. A close reader looking for how to do genomics would be better served reading the actual research paper. Here, I'm trying to express the science for everyone else.

By 1930, R. A. Fisher picked up Darwin's idea about numbers, predicting that evolution in large populations could be faster than in small populations. However, this is not in all circumstances, but only where the number of new adaptive mutations is quite small -- in other words, where evolution is "mutation-limited":

The great contrast between abundant and rare species lies in the number of individuals available in each generation as possible mutants.... The importance of the contrast lies with the extremely rare mutations, in which the number of new mutations occurring must increase proportionately to the number of individuals available.

A long history of research in plant genetics (corn breeding), microbial chemostat experiments, and the examination of pesticide resistance in insects support Fisher's concept. For example, flies subjected to low doses of pesticide in the laboratory tend to acquire very complicated patterns of resistance -- involving slight changes in many different genes. These usually aren't transmitted perfectly and often have fitness costs; it's a very imperfect adaptation. But if pesticide is sprayed over a large area, flies sometimes appear very quickly with a single mutation that confers very complete resistance. Here, the very advantageous resistance mutation is incredibly rare -- it only occurs in maybe one in a billion flies. It would never occur in the small laboratory population.

Our growing population

Human populations have been growing rapidly during the last 50,000 years or so. That increase began around the time of the Upper Paleolithic -- that's documented by archaeological evidence. There was a later massive increase during the Neolithic. This agricultural transition actually was quite heterogeneous: earlier in West Asia and China, later in Europe, and then later still in subsaharan Africa. Last, we have within the last few hundred years seen a massive increase in numbers associated with industrialization and globalization of technology.

One day a couple of years ago, Greg Cochran and I were talking about brain evolution. You have to understand, this is long before we knew about any of these genome scans -- they hadn't come out yet. One of the main mysteries of human brain evolution is why it happened apparently gradually for such a long period of time. It is one of the best cases of evolutionary gradualism. But this is a problem, because directional selection would have too be too weak to take such a long time. Now, we know that brain size is constrained in two directions -- larger brains cost more energy to maintain, but smaller brains come with some functional disadvantages. So this creates a situation where new variants that satisfy both constraints -- costing little energy, or making great improvements in brain function -- must be very rare. It should be mutation-limited.

I remember very well, that at precisely the same moment, we both realized -- "Hey, maybe this great increase in human population size made a difference!" Because as we'll see later, the pattern of change in brain size really changed when populations started to get really big.

You see, this is one of those very rare cases where the theory preceded the data! It is quite simple; the rate of mutations in a population is a linear product of the rate per genome and the population size.

Not all mutations are advantageous, and not all advantageous mutations will be fixed. The vast majority are lost. If a mutation has a selective advantage, then the chance that it will proceed toward fixation (and attain high frequency) is 2s -- "s" here is the fitness advantage. That means that 90 percent of new mutations with a 5 percent fitness advantage are simply lost.

The most beneficial mutations are very rare; it is much more likely that a new mutation will be weakly selected. This is another aspect of selection that has been well-known since Fisher. So the chance of fixation increases with s, but the likelihood of the mutation decreases with s -- in fact, the number decreases exponentially as selection is stronger and stronger.

If you put all these together, you can predict how many selected changes you should see in a population that has been growing in size. This tells us the number of new adaptive mutations that should come into the population each generation. It is still linear with population size -- a larger population should have more mutations in precise proportion to its size.

Still, a very small fraction of the mutations in any given population will be advantageous. And the longer a population has existed, the more likely it will be close to its adaptive optimum -- the point at which positively selected mutations don't happen because there is no possible improvement. This is the most likely explanation for why very large species in nature don't always evolve rapidly.

Instead, it is when a new environment is imposed that natural populations respond. And when the environment changes, larger populations have an intrinsic advantage, as Fisher showed, because they have a faster potential response by new mutations.

From that standpoint, the ecological changes documented in human history and the archaeological record create an exceptional situation. Humans faced new selective pressures during the last 40,000 years, related to disease, agricultural diets, sedentism, city life, greater lifespan, and many other ecological changes. This created a need for selection.

Larger population sizes allowed the rapid response to selection -- more new adaptive mutations. Together, the the two patterns of historical change have placed humans far from an equilibrium. In that case, we expect that the pace of genetic change due to positive selection should recently have been radically higher than at other times in human evolution.

Finding selection in the genome

Now, it comes to a problem of how we can see recent mutations that have been selected. A genome scan is based on things that vary, not things that are fixed. So we are looking at some window of frequencies. In our study, that was a window from around 22 to 78 percent.

Before we go too far, it is important to point out that an adaptive gene will be in a window where we can detect it for only a short time -- it spends a long time getting up to an appreciable frequency (here 22 percent, which is our lower ascertainment bound) and a long time going from a high frequency (here 78 percent) to fixation -- this is for a dominant. But it spends only a very short time in the window where we can see it.

And strongly selected genes go through this window quite a lot faster than weakly selected ones.

The importance of this is that we will see genes with different strengths of selection at different ages. Our constraint is that right now all the things we can see are variable -- but some are variable because they originated a short time ago and were very strongly selected, and others are variable because they originated a long time ago, but were very weakly selected.

You can guess, that we expect to see more of the weak ones than the strong ones, because there should be more of them! So the window should give us a view of the strength of selection as well as the number of mutations. If we can estimate the ages of our mutations, then we can predict how many there should be at different strengths of selection, and try to quantify the effect of population size.

Here, we've drawn a graph showing the number of genes in the window, compared with the number that are still variable in the population -- they are on their way to fixation -- but they are outside the window. This is for a growing population, so you see that the number of these genes increases as you get closer to the present.

There are many more that we can't see than the ones we can see -- this is like the tip of the iceberg. That is one aspect of recent selection; these genes are in this intermediate frequency range for a short time, and there will be many more genes that are too rare for us to see with our current methods, but might be very important regionally or locally in some populations.

Based on a model of population growth, we expect to see a big peak corresponding to the period when humans were growing rapidly during the Neolithic. The distribution should plunge down toward the present, because selection would have to be so strong on such a recent mutation for us to see it -- we're talking about 20 percent or more. Those just almost never happen. The true number, remember, is the iceberg under the water -- but we must make predictions about the part we can see.

Linkage disequilibrium and selection

Now, I need to say a few words about how we find these genes when we scan the genome. The International HapMap consists of a list of over 3 million genetic polymorphisms -- SNPs -- taken from a sample of people with ancestry in Northern Europe, West Africa, and East Asia. When we look at a sample of a long stretch of DNA from several people, we will be considering the frequency of many different polymorphisms.

But more important, we have studied whether each polymorphism is linked to the others. As a new positively selected allele increases in frequency in a population, it is initially linked to a wide region including many nearby polymorphisms. This induces a long-distance association among SNPs, which is called linkage disequilibrium.

When we are looking at a stretch of chromosome, what we can observe is that there are areas where recombination seems to be very rare around one SNP -- an in particular where one of the two SNP alleles has almost no recombinant chromosomes, but the other allele appears to have been recombining normally. That kind of mismatch is a strong indication of selection.

I'm not going into the details of that process right now; I'll be posting some real examples of such LD decay analyses later in the week. After applying the analysis, we found more than 3000 in the Yoruba sample, more than 2800 in Europeans, and more than 2300 in Asians.

These numbers are very large -- they make it look like this aspect of evolution, positive selection on new adaptive alleles, has been going very fast. But how long a time period are we looking at? Based on the local rate of crossing-over, we can say how quickly LD ought to be broken by new recombinations, and that allows us to derive age estimates. The ages represent the time that has elapsed since the initial mutation that established each adaptive allele.

Here is a comparison between the ages of selected variants in the African HapMap and in the European HapMap. Let's look at this graph a little bit.

Each of these dots represents a number of different genes -- the y-axis is number; this is a histogram. The x-axis is the age. So you see, there are many of these selected genes that started around 10,000 years ago; there are many fewer that started around 40,000 years ago, and even fewer starting 80,000 years ago.

These fitted lines are what you get if you fit a one-parameter model with very strong selection to these curves. You can fit these without considering the effects of population growth.

But you notice some differences here between the African and European distributions. Africa has a few more total variants, but it especially has more older variants, before 10,000 years ago. You can see that during that time period, Europe has very few. And Europe has this later peak, where we see an earlier peak in Africa.

These details are a very good match to demographic growth -- Africa had much larger population size during the Late Pleistocene than Europe, but West Asia, and then Europe had earlier Neolithic expansion than Africa -- so we see these early times have a lot more selected variants within Africa, and later on there is a pulse of adaptive variants in Europe.

Testing acceleration

At this point, we have a theory that predicts acceleration of new adaptive variants, and we have data that appear to show a very fast recent rate. But we haven't yet directly tested the hypothesis of acceleration.

We chose a null hypothesis approach. After all, the rate of change looks like it has been very high recently, but what it if were always very high. A constant rate of change is a null hypothesis -- the hypothesis of no change, or in our case, no acceleration. So we worked out the predictions of this hypothesis: a constant, high rate of selection. If we could show that those predictions aren't true, then we could disprove the null hypothesis and show that adaptive human evolution accelerated.

We took several different approaches, testing predictions on different kinds of data. For one thing, if the null hypothesis were true, then there should be a whole lot more selected mutations that have already reached or approached fixation, than the relatively small number that we see still varying in human populations. So to test the null hypothesis, we should look for evidence of these fixed selected substitutions.

That's exactly what we did -- we looked at other means of assessing the number of recently fixed and near-fixed variants.

On the bottom of this graph, we have the European age distribution of variants in our window. This should represent a small fraction of the total number that have happened across this time period. But you can see from this graph, that if the rate was constant, the total number should be very, very large -- since we are looking at 10-generation bins, here we have around 150 predicted substitutions every 10 generations, or around 1/2 per year. Most of these should be way above our window, in fact, as we go back toward 40,000 years ago, almost all should be close to or at fixation.

This large number of completed sweeps should have vastly reduced human genetic variation, because polymorphisms tend to hitchhike along with nearby selected alleles. Hitchhiking up to fixation tends to eliminate variation. When we look at the effect of hitchhiking under this constant selection hypothesis, the genome-wide average diversity should be less than a tenth of what we actually observe. So that also disproves the null hypothesis.

How much acceleration?

Down at the bottom of the graph, you see the predicted number of selected variants over our window, under the hypothesis of population growth -- exactly the demographic growth that really happened to humans. And here you see, that there are many, many fewer of these predicted, and in fact over the long course of human evolution, the rate would have been very low.

We can put a number on just how low, and when we do that, we can see how much human evolution has sped up. For example, if we have 1/2 of a substitution per year, well, there are around 12,000,000 years separating humans and chimpanzees (6 million since the common ancestor, in both these lineages). So if adaptive substitutions had happened at a constant rate as high as the last few thousand years, we should be looking at around 6 million fixed adaptive substitutions between humans and chimpanzees.

But in reality there have been nowhere near that number. There are only 40,000 total amino acid substitutions between humans and chimps. Not all those were selected -- maybe only a third. We can add in some additional selected sites outside of coding regions, but still we are looking at an increase in the rate of new adaptive mutations in humans that is 100 times faster than could possibly have been true during most of human evolution.

Our evolution has recently accelerated by around 100-fold. And that's exactly what we would expect from the enormous growth of our population.

What is all this selection for?

We know something about the functional categories of genes inferred to be under selection; we are studying this now. We expect it will keep us busy for some time.

In a general view, they illustrate the idea that changing cultures and ecologies have been important in changing the pattern of selection. For example, many of the selected genes are involved with pathogen defense -- for new pathogens that didn't always exist. Some are apparently related to metabolism or even directly to diet, in terms of processing new food sources. Of course, lactase is an excellent example in this category.

These are not the kinds of phenotypes that have a lot of visibility in skeletal remains. But we have a skeletal record of these populations during the last 40,000 years. We know a lot about what they looked like and how they changed. So we may try to relate the pattern of genetic, skeletal, archaeological, and other kinds of changes over time.

One obvious way to test hypotheses about these changes would be to sample ancient DNA from skeletons. In this way, we could see if the new selected alleles are in them or not. This spring, a paper by Burger and colleagues (PNAS) sampled ancient European skeletons, Neolithic skeletons, for the lactase persistence allele. They didn't find any who had that allele -- not a single one, and this is in Neolithic populations where today the allele is up over 90 percent in frequency. What is going on there?

In this case, it is quite obvious by considering population genetics. We have a very good date for this lactase persistence allele, from many sources -- it is around 6000-10,000 years old. And you can see in the figure, a new selected allele will remain at a very low frequency for a long, long time after its origin. Here, these skeletons were sampled at a time when the selection pressure favoring the allele was present, but the allele had not yet increased to a substantial frequency. In fact, this allele would have been rapidly increasing through these intermediate frequencies much more recently -- we're talking here about Roman times. And today it is over 90 percent in Scandinavia, but considerably lower in Italy and Southern Europe.

In the future, we will be able to sample for genes more widely in ancient skeletons. At the same time, we will be able to sample skeletal changes to try to correlate them with allele origins. That is some research that I have applied for a number grants to support, and I think it will be very promising.

Conclusion

I hope that this essay gives an introduction to the work we have done. This was based on a presentation about the research I gave earlier this year. There are many missing ends, and I'll be adding more information over the next several days about ways of testing for selection, as well as some of the more surprising implications of our research. I've written it without a bibliography, which I can direct you to the paper for a full set of references.

The embargo has now ended on the second, and far more important paper that I mentioned the other day. It is a product of work I've been doing with Bob Moyzis of UC Irvine, his former graduate student Eric Wang, now at Affymetrix, my friend Greg Cochran and Henry Harpending at the University of Utah.

Some readers may know I've been working on this project -- I've given presentations at meetings and at a number of universities about it. But otherwise I've been silent about it. In particular I have been systematically avoiding the topic of recent selection here on the weblog. It has been a great inconvenience to me, but the unhappy fact is that journals want new results, and blogging about something is at least perceived to reduce its news value. And of course, working with other people across the country entails a lot of respect for keeping discussions and results confidential until we have all signed off on everything.

Anyway, I'm hugely excited about this project, our current results, and what we will be doing next. Which means I have some pent-up writing to do! Over the next few days, this will be acceleration central -- I'll be laying out what these genomic data mean for recent human evolution, what kinds of genes we have been finding under selection, and exactly how these kinds of analyses are done.

I'll also be tracking press articles and blog reactions to the paper. PNAS is, if anything, consistently unpredictable about when they actually make papers available. If you want a preprint, please let me know. I'd also appreciate your links.

Also, if you've come here for the first time, welcome! I may get a lot of traffic for a few days, so I apologize if things are slow.

Here's a start: the abstract.

Recent acceleration of human adaptive evolution

John Hawks, Eric T. Wang, Gregory Cochran, Henry C. Harpending, and Robert K. Moyzis

Genomic surveys in humans identify a large amount of recent positive selection. Using the 3.9-million HapMap SNP dataset, we found that selection has accelerated greatly during the last 40,000 years. We tested the null hypothesis that the observed age distribution of recent positively selected linkage blocks is consistent with a constant rate of adaptive substitution during human evolution. We show that a constant rate high enough to explain the number of recently selected variants would predict (i) site heterozygosity at least 10-fold lower than is observed in humans, (ii) a strong relationship of heterozygosity and local recombination rate, which is not observed in humans, (iii) an implausibly high number of adaptive substitutions between humans and chimpanzees, and (iv) nearly 100 times the observed number of high-frequency linkage disequilibrium blocks. Larger populations generate more new selected mutations, and we show the consistency of the observed data with the historical pattern of human population growth. We consider human demographic growth to be linked with past changes in human cultures and ecologies. Both processes have contributed to the extraordinarily rapid recent genetic evolution of our species.

This is a bold assertion, and I will be putting out an FAQ later today that covers many of the questions I have been fielding from the press. There is a lot of technical detail in it, but we have accomplished essentially two things:

1. An empirical age distribution for alleles under recent selection, which number in the thousands.

2. A theoretical account of why these new alleles should have been increasing rapidly in numbers during the last 40,000 years.

It is a powerful paper because it shows why a rapid acceleration of our evolution is expected in theory, and it matches those expectations to real empirical data. It shows the absolute impossibility of a constant rate of selective change in humans, and that gives reality to our estimate of the amount of acceleration.

The last paragraph of the discussion:

It is sometimes claimed that the pace of human evolution should have slowed as cultural adaptation supplanted genetic adaptation. The high empirical number of recent adaptive variants would seem sufficient to refute this claim. It is important to note that the peak ages of new selected variants in our data do not reflect the highest intensity of selection, but merely our ability to detect selection. Due to the recent acceleration, many more new adaptive mutations should exist than have yet been ascertained, occurring at a faster and faster rate during historic times. Adaptive alleles with frequencies under 22% should then greatly outnumber those at higher frequencies. To the extent that new adaptive alleles continued to reflect demographic growth, the Neolithic and later periods would have experienced a rate of adaptive evolution more than 100 times higher than characterized most of human evolution. Cultural changes have reduced mortality rates, but variance in reproduction has continued to fuel genetic change. In our view, the rapid cultural evolution during the Late Pleistocene created vastly more opportunities for further genetic change, not fewer, as new avenues emerged for communication, social interactions, and creativity.

Over the next few days, I'll fill you in a bit about the course of this research -- how we got started, how it proceeded, and what parts of it remain exciting. Also, I'll try to give a flavor to what genomics means for anthropology -- what exactly is "anthropological genomics?" I think that there is an exciting frontier opening in the way we look at the past, and I hope to be able to show how some of it will work over the next few years.

Although I've had a number of papers come out this year, there are two in particular that I've been working on for quite a long time. Both papers began their gestation in the summer and fall of 2005. Each of the two papers explicates a major pattern for the action of natural selection in human evolution -- to my mind, at least, the most important two. Each was a long project, requiring the integration of mathematical, theoretical and informatic resources, and researchers scattered across the country.

Both papers were submitted earlier this year to different journals, and in several instances revisions and decisions about them were made within a week of each other.

Now, the two papers are being published online, both within a week of each other.

The first to appear is our review of genetic introgression and modern human origins, now online in Trends in Genetics.

Gregory Cochran and I published a number of theoretical considerations about introgression last year (Hawks and Cochran 2006, described in this post). That paper included a very comprehensive review of adaptive introgression among natural populations, focused on mammals, citing more than 170 references. But we had relatively little to say about the genetic evidence for introgression in human evolution, because the key paper from Bruce Lahn's lab (Evans et al. 2006) had not yet been published.

We have included some of that evidence in our current review. It is a shorter, more compact paper than last year's. That means that it leaves out a number of details, but it allows us to bring the molecular evidence and population genetic theory together.

In that form, it is possible to discuss some of the interesting predictions we might make about Neandertal-human population dynamics. For instance, why are two of the candidate introgressive alleles related to the brain? Our final section, "What did archaics have to offer?" takes on this question:

Adaptive alleles from archaic humans present a paradox. We recognize archaic humans by their morphology, and their morphology has mostly disappeared. Therefore, if moderns still retain adaptive alleles from archaic humans, those alleles almost certainly were not correlated with traits that we recognize as archaic. Instead, they must be related to phenotypes that we cannot recognize easily in archaic human fossils.

This is a crucial fact. We already know that Neandertal anatomies disappeared. But what makes a "Neandertal" anatomical feature? Clearly, we recognize it precisely because it is rare today.

If we are going to look for introgressive alleles, we have to look outside of this acquisition bias. The brain is a promising area on this score -- we know little about its variation in fossil humans.

In the final section, we allowed ourselves some speculation about the dynamics of modern human origins and dispersal:

Cosmopolitan populations like modern humans are generally a threat to endemics, but this threat intensifies during range expansions and population growth. In endemic species, alleles that promote outbreeding can be selected merely because the cosmopolitan species is expanding, aiding the collapse of former reproductive boundaries. Certainly, the distinctive morphological adaptations of archaic humans lost some of their selective advantage with the increasing technical sophistication of the early Upper Paleolithic (35 000 - 15 000 years ago). This must especially have been true of populations like the Neanderthals, whose skeletal and muscular specializations required a high energy budget. In an adaptive context, Neanderthals and other archaic humans were like endangered endemics, suffering from relatively high mortality and high energetic costs. Possibly, the only remaining adaptive strategy for them was mixture with the more cosmopolitan modern humans.

This is of course speculative, but I think it is valuable because it attempts to place ancient human populations in the context of modern conservation biology.

We often read that various human groups were "endangered" at one time or another, including the Neanderthals. But I have not seen anyone take the next logical step, which is to discuss the ways that endangered species actually interact with their congeneric competitors. When the interaction between populations includes interbreeding, interesting dynamics may emerge.

Does this mean that humans and Neandertals were distinct species who intermixed by hybridization?

I wrote about that question last year, concluding:

There will never be any tidy solution to the species problem, because all species have unique evolutionary histories and constraints. Given these difficulties, the species status of archaic Homo populations is basically an intractable problem. That is, I am happy to suggest that archaic Homo populations correspond to classical subspecies, and as far as I know, no evidence strongly contradicts that position. But I can recognize that some people will never agree with this assignment. And from the perspective of their evolution, it just doesn't matter. Evolutionarily important gene flow occurs between mammal species, subspecies, and populations.

The last sentence is the most important point. Those who want to put Neandertals into a distinct species (Homo neanderthalensis) generally believe that there was no evolutionarily significant gene flow between them and modern humans. But the opportunity for evolutionarily significant gene flow is always there, irrespective of whether the populations are species, subspecies, or even genera. Remember Bos-Bison introgression.

You can't simply define the problem of Neandertal-modern interactions away by giving them different names. And in reference to the "paradox" pointed out above, there is no defining the problem away by pointing to morphological differences. If we recognize that Neandertals are hominids, that is quite enough to suggest that gene flow was possible between them and their contemporaries.

The only thing left is to quantify the amount. The genetic observations thus far suggest that a predominant fraction of the gene pool of living humans descends from a relatively homogeneous ancient population. Since Late Pleistocene humans were geographically differentiated, this means that one ancient population disproportionately expanded at the expense of others. Genetic comparisons allow us to infer that the expanding population was initially African. This expanding population received introgressive alleles, both from other African populations and from Eurasian ones.

But that was not the end of the story. Introgressive alleles succeeded or failed on the basis of selection on them. The expanding population continued to grow in numbers. And the stage may have been set for something even more interesting...

More reading

"Why introgression?" discusses why introgression is a useful concept, compared to the simpler "gene flow."

"Introgression and microcephalin FAQ" addressed the MCPH1 genealogy.

"Neandertal introgression, anatomically" reviewed the paper by Soficaru et al. (2006) on the Pestera Muierii skull.

"The inevitability of introgression" announced and gave some details from our 2006 paper.

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 103:18178-18183. doi:10.1073/pnas.0606966103

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 (early online) doi:10.1016/j.tig.2007.10.003

I noticed that the cover of the most recent New Scientist is a story about modern human origins by science writer Dan Jones. It's headlined, "Going global: how humans conquered the world."

I think Jones has done a nice piece of work here -- at 2700 words, the story is easy to read, and it illuminates a certain kind of current consensus. It touches on everything from the Herto hominids, to the Blombos The underlying theme is the idea of a "coastal route" dispersal of modern humans from Africa, coupled with some detail about Paul Mellars' Afro-Indian connection, Spencer Wells' Y-chromosome story, the early Herto and Omo Kibish remains, the relevance of Oase and Tianyuan to early dispersal scenarios, and the "megadroughts" of the African Late Pleistocene.

I'll tell you one thing: The piece succeeds at making me feel like a member of the Neandertal Underground, standing on the side of the road as the march of the "Human Revolution" goes by.

The thing is that none of these separate elements fit together. It's not hard to figure that tracing the Y chromosome genealogy of Eurasia to a divergence in the Middle East 40,000 years ago doesn't match up very well with the idea of an "early coastal route dispersal" 60,000 years ago, or an initial colonization of Australia 50,000 years ago. Placing "modern human anatomy" earlier and earlier in time -- back to 200,000 years ago -- isn't exactly helping to explain the behavioral record in the last 70,000 years. And the archaeology that places "modern human behavior" increasingly into the Middle Stone Age doesn't explain why the same behaviors should be found in Neandertals.

Sometimes the contradictions are so glaring that Jones almost can't help but juxtapose them:

"The similarities between Africa and India are not coincidental, and fit in beautifully with the DNA evidence," says Paul Mellars, an archaeologist at the University of Oxford. Although none of these artefacts is more than 35,000 years old, that may simply reflect the fact that sea levels are about 100 metres higher today than they were 50,000 years ago. Any artefacts or bones left by the first coastal migrants are now buried beneath the sea.

I never credit someone with quotes taken from a news article -- every nuance of the evidence is simply not that important to the casual reader. But it's sort of obvious that some of the DNA evidence poses a problem here. And the dates are entirely discordant.

Mellars has emphasized in print (e.g., 2006) the material similarities between early Upper Paleolithic assemblages of India and the Howieson's Poort industry of Africa. The similarities are there, but the dates are quite different. "Lower sea levels" is only arm-waving: Sure, the lack of earlier evidence of similar industries is a problem, but a much bigger problem is explaining the 40,000-year persistence of these "similar" industries in the constant adjacent presence of other patterns of material culture.

The obvious alternative is that the similarities are coincidental -- or at least don't reflect a lineal cultural relationship between 70,000-year-old Africans and 30,000-year-old Indians. That doesn't argue against dispersal: after all, the abilities represented by the material remains may have dispersed, early or late, even if the tools themselves didn't.

But we should also consider the similarities with the cultural remains of late Neandertals and even earlier peoples of Europe, including the pigment use, engraved lines, pendant drilling and blade manufacture.

What we have here is a clown car of a hypothesis: everything thrown in but the bearded lady. No hypothesis is ever tested: Consistency rules. This is no discredit on Jones at all, who clearly does the best job possible of fitting together all these recent papers. The problem is that when you see them all next to each other, you can't help but see that these 115,000-year-old Eritrean shellfish, 40,000-year-old Y chromosome divergences, 65,000-year-old mitochondrial haplogroups, 30,000-year-old Indian blades, 35,000-year-old Romanian skeletons, 70,000-year-old ochre engravings, and 190,000-year-old African skulls really can't fit together to tell a story of a single human dispersal at a single time.

Either the hypothesis is wrong, or some of the data are. Or both.

References:

Jones D. 2007. Going global: how humans spread across the world. New Scientist, Oct. 27, 36-40.

Mellars P. 2006. Going east: new genetic and archaeological perspectives on the modern human colonization of Eurasia. Science 313:796-800. doi:10.1126/science.1128402

This week, Johannes Krause and colleagues from the Max Planck Evolutionary Anthropology institute announced that they had tickled FoxP2 out of two Neandertal specimens from El Sidrón, Spain. The bones were excavated in sterile (clean-cave?) conditions, immediately frozen and then shipped to Leipzig, where extracts were taken in clean-room conditions.

Here's an FAQ about what they found.

Why is this paper really important?

Isn't it obvious? It's important because it demonstrates that more than one Neandertal is suitable for nuclear genome recovery. We will know about genetic variation in Neandertals, sooner rather than later. These two bones come from different individuals, because the Leipzig group found two different mtDNA sequences in them. Together with the Vindija Vi 33.16 specimen in the original Neandertal genome papers, this makes three nuclear genome Neandertals. There will be more.

It also shows the possibility of probing ancient skeletons for specific genes. Here, they went in looking for Y-DNA, X-DNA and particular sites on FoxP2, and they found them. That is definitely the way to go if you want to test a biologically significant hypothesis fast -- otherwise, you just have to wait until the sequence comes up in your genome project.

However, I question the value of probing for individual genetic variants in this way. Every probe takes a bit of sample, which might be more efficiently used in whole-genome sequencing. We have 25,000 genes, and every one is potentially interesting. Every small sample used to assay only one of those genes may destroy many sequences from the others. It would be one thing if samples were trivial and easily replaced, but they obviously aren't.

Still, we will certainly see additional probes for genes that are of particular interest. I wouldn't be surprised to see MC1R results soon, to probe whether there were pigmentation variants in Neandertals. The same has already been done for woolly mammoths.

So, Neandertals had the human-specific FoxP2 form. Did they talk?

I think the genetic observation leans toward that direction, but doesn't really change our understanding. Consider:

Neandertals have a hyoid bone with humanlike anatomy, as did the Atapuerca people at more than 300,000 years ago, even though A. afarensis did not. So something related to vocalization evolved in humans by the Middle Pleistocene. Although Neandertal vocal tracts may not have been identical to recent humans, there is nothing about them that would preclude speech. The only paleoneurological observation about language puts a developed Broca's area on the KNM-ER 1470 endocast, Homo habilis.

Like other Middle Paleolithic/MSA people, their technology required more information to learn than earlier, Lower Paleolithic industries, leading to regional differentiation and more task-specific facies. Late Neandertals made use of some technology otherwise used only by Upper Paleolithic modern humans. Their hunting methods must have required cooperation and may have been impossible without a more sophisticated communication strategy than used by other primates.

All of these things argue for some kind of Neandertal language irrespective of FoxP2.

Then again, most of the arguments against humanlike language facility in Neandertals also have nothing to do with FoxP2, either. The slow technological progress, limited collection strategies, the rarity of any artistic or symbolic expression, their high mortality rate, and -- of course -- the fact that they no longer exist have all been considered as evidence that Neandertals lacked some essential aspect of "behavioral modernity." If language is a prerequisite for the modern human pattern of behavior, then Neandertals may not have talked, at least not in the way we do.

I think the FoxP2 story has really confused people much more than necessary. But in this case, the confusion is the same that results from every other gene study: when the press says we've found a gene "for" something, what it ought to say is that we've found an allele that affects something.

No macromutation happened. Language did not spring full-formed into the mind of some ancient African. All members of Homo used communication systems including some (possibly minimal) elements of language, and the evolution of the human brain, along with technological changes throughout the Paleolithic, reflect the evolution of communication. Human language evolved -- like all things -- over a long time, and like all complex phenotypes it required a series of mutational changes. Many of these mutations became fixed during recent human evolution, some may still be changing in frequency today. Language evolution is probably a continuing process.

That means that it must have involved many more genes than FoxP2 -- which after all experienced only two amino acid substitutions in all of human evolution. I would imagine the number of genes involved in language evolution is more than 500, and I wouldn't be surprised if it were much more. In that context, it seems quite silly to say FoxP2 is the "critical" evolutionary change for anything.

Then you agree with Language Log. They told me that FoxP2 isn't a "language gene."

The case is strong that the two FoxP2 coding substitutions in humans were selected because of their role in language. The gene sequence is strongly conserved in most mammals, and shows similar changes in some other species with unusual vocal adaptations, such as echolocating bats (Li et al. 2007). Its expression pattern delineates areas related to vocalizations in both humans and birds, and the pattern itself differentiates between song-learning versus nonlearning bird species (Haesler et al. 2004, Teramitsu et al. 2004, Webb and Zhang 2005). And of course, mutations to FoxP2 can result in specific language impairment (SLI) in humans.

Still, that case is only circumstantial. We know that FoxP2 was under selection, that it became fixed in humans, probably during the Late Pleistocene, and that breaking the gene changes brain development and damages language skills. But we don't know what a human would be like with the chimpanzee form of the protein. We don't know whether both of the human-specific amino acid substitutions have a different effect than one. Most important, we don't know what other genetic changes may have been necessary backgrounds for selection on FoxP2.

This means Neandertals were really modern humans, right?

This study should put an end to the "sudden mutation" model of modern human origins.

There was not a single mutation that made the critical difference in the ancestry of today's people. There was no cognitive Rubicon leading to modern human evolution. I would analogize the process as a slow-motion avalanche: at first a few small sands began to tumble, and then selection on a large number of genes became inevitable. FoxP2 is one of those genes, and as yet we don't know whether it was near the beginning or near the end of the process.

But it is clear that the process began before the Neandertals were gone. Some aspects of behavioral complexity did begin to evolve rapidly sometime after 70,000 years ago. This rapid evolution was multiregional in context -- it was not limited to a single human population. In particular, it was not limited to Africans: the last Neandertals clearly manifested technological and behavioral strategies otherwise defined as "behaviorally modern" (d'Errico 2003). There's a reason why the Neandertal-produced Châtelperronian industry of France and Spain was historically considered the first Upper Paleolithic industry.

But we have undergone light-years of change since the last Neandertals lived. This is not a question of "modern human origins" anymore. We can now show that living people are much more different from early modern humans than any differences between Neandertals and other contemporary peoples. I think that "modern humans" is on its way to obsolescence. What matters is the pattern of change across all populations. Possibly that pattern was initiated by changes in one region but the subsequent changes were so vast that the beginning point hardly matters.

We all know that the Neandertal genome is riddled with contamination from modern humans. Isn't the null hypothesis that we have a modern human sequence here because it is a modern human?

Well, as you know, I'm not all that convinced that contamination explains the interpretive discrepancies between last year's genome papers. But still, this study has done some things to address the problem of contamination.

It is notable that Green et al. (2006) found 25% modern human mtDNA in one of the El Sidrón bones: this shows that even "sterile" excavation, immediate freezing and extraction under clean-room conditions cannot exclude contamination. There is at the moment nothing more that can be done. We will always have the problem of a contamination fraction in ancient Neandertal skeletons. So we have to judge each study by the extent to which we can exclude contaminants with statistical analysis.

For this study, Krause et al. (2007) developed a test of nuclear DNA contamination: they identified seven gene variants that differ between the recovered Vindija Vi 33.16 nuclear genome and all known living humans. In other words, these are human-derived mutations that are absent from the only known Neandertal nuclear genome. Then, they probed the El Sidrón bones for these sites. They found only the ancestral form in their extracts of both bones -- presumably because no human contaminants were present in their samples.

That seems like a pretty good indication that the other sites in their sample represent the true gene variants o