Holocene

The NY Times reports on evolution and education in Texas:

Starting this summer, the state education board will determine the curriculum for the next decade and decide whether the "strengths and weaknesses" of evolution should be taught. The benign-sounding phrase, some argue, is a reasonable effort at balance. But critics say it is a new strategy taking shape across the nation to undermine the teaching of evolution, a way for students to hear religious objections under the heading of scientific discourse.

Already, legislators in a half-dozen states -- Alabama, Florida, Louisiana, Michigan, Missouri and South Carolina -- have tried to require that classrooms be open to "views about the scientific strengths and weaknesses of Darwinian theory," according to a petition from the Discovery Institute, the Seattle-based strategic center of the intelligent design movement.

The story mainly covers the local Texas aspects of the story, with quotes from the state education board chairman ("I believe a lot of incredible things") and some pro-evolution opponents.

I looked at the website where the Texans for Better Science Education lay out examples of the "weaknesses" that should be taught. They're pretty weak, all right. I think that most of these could be included in a science course as "common myths about evolutionary theory."

Consider these:

The Cambrian explosion quickly produced all of the basically different body structures, and some of these have since become extinct. This is very different from the evolutionary tree of life, which suggests a slow and gradual increase in body structures.

No, no it doesn't. Evolutionary theory provides no reason to think that body structures should change at a slow constant rate. The synthetic theory emphasizes why bursts of adaptive change should happen episodically.

Many life forms persist through large expanses of geologic time with essentially no change. Evolution theory suggests that mutations occur randomly over time and are selected to produce continuing change as the environment continually changes.

No, no it doesn't. Some organisms may well have relatively constant environments for millions of years.

Selective breeding has produced only very limited change with no new structures occurring over thousands of years and multitudes of generations of selection.

Umm... teosinte? I think that biology texts should devote a lot more attention to selective breeding, as the best concrete examples of evolution in action.

So, that reflects on the basic problem with the idea of teaching evolution's "weaknesses": A real weakness is not a matter of ignorance, but a matter of evidence weighing in favor of some alternative hypothesis. We don't have that here.

That's the thrust of a technical comment by Graham Coop and colleagues, now online in Molecular Biology and Evolution. The letter refers to the extraction of FOXP2 from two Neandertal specimens from El Sidrón, by Johannes Krause and colleagues, reported last year (I wrote about the paper here).

First, the bad news. The current letter raises the prospect of contamination. Notably, the controls applied by Krause et al. (2007) may be relatively weak evidence against contamination, because of polymorphism within large human comparative samples. The tests rely on the assumption that there is little DNA from living humans in the samples. But if we cannot distinguish Neandertal from human DNA with great accuracy, then we will be mistaken some proportion of the time. Krause et al.'s test, based on derived human alleles absent from the Neandertal genome draft, can still go wrong if the human contaminants happen to have all the ancestral (non-derived) human alleles.

Well, that seems to be the story these days with Neandertal DNA extraction. No test of contamination is good enough. (And remember, that every "test" of contamination is really a procedure for excluding the hypothesis that ancient sequences are identical to recent ones.)

Now, the more interesting news. Coop and colleagues verify that the selective sweep affecting human FOXP2 was indeed recent -- they estimate 42,000 years ago:

To demonstrate this, we estimated the time of the most recent common ancestor (tMRCA) of the selected haplotype (see Figure 1), using an approach sometimes called phylogenetic dating (Thomson et al. 2000; Hudson 2007). This method does not make assumptions about demography and selection, but only requires that the mutations in the intron be neutral or nearly neutral. Taking this approach, we obtained a mean tMRCA of 42 Kya (see SOM for details). While there is considerable uncertainty associated with this estimate, it is surprisingly recent if selection took place over 300 Kya (see SOM). In other words, the selective scenario proposed by the authors cannot account readily for patterns of variation in modern humans. Given that we have no power to detect a beneficial substitution that occurred over 250 Kya, (cf. Sabeti et al. 2006) yet we see a footprint of positive selection at FOXP2, the conclusion of a recent selective sweep at FOXP2 is not surprising (Coop et al. 2008:3-4).

FOXP2 is in one of the ENCODE regions, so its variation is pretty well known. This is not a problematic case: it has a very limited amount of variation around it, and has a strong excess of rare alleles, both signs of a recent sweep.

Coop and colleagues suggest that the beneficial human allele spread into Neandertals (or vice versa) by low levels of gene flow coupled with its selective advantage -- in other words, introgression.

They do allow for an alternative -- perhaps the two amino-acid-coding mutations were not the target of selection, but instead some linked locus. This would not erase the necessity of gene flow from Neandertals, but would question whether this gene flow had involved the FOXP2-language scenario, since it might be some linked gene unrelated to language.

(CORRECTION (2008/04/18): If selection were on a linked site, then Neandertals might share the human-derived amino acids as a result of ancient shared ancestry with humans, while the linked selected sweep might be absent in Neandertals, not necessitating any gene flow.)

I doubt this hypothesis of a linked sweep, since the two sites with human-derived substitutions are otherwise very strongly conserved among mammals. This looks like a credible target for recent selection. But the hypothesis of selection on a linked site cannot presently be tested.

So that's the story. It seems very likely that Neandertals got the language gene from us, or us from them, long after many other genes in the two populations diverged. I write "many" rather than "most" because we haven't really been able to assess the proportion of derived alleles shared by humans and Neandertals. The completion of the draft sequence may help, but I'm afraid that the specter of contamination is going to keep on being raised whenever a part of the Neandertal draft genome looks humanlike.

(via Dienekes)

References:

Coop G, Bullaughey K, Luca F, Przeworski M. 2008. The timing of selection at the human FOXP2 gene. Mol Biol Evol (in press) doi:10.1093/molbev/msn091

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.

That was the message that just flashed surreally on my TV screen, from the old U2 "ZooTV" tour. Yes, that's the one where the Edge is wearing a beret.

So, having this excellent 17-year-old advice from Bono, I decided to Google "EVOLUTION IS OVER" to see what I would find.

Here's an old article (2002) in The Observer by Robin McKie:

For those who dream of a better life, science has bad news: this is the best it is going to get. Our species has reached its biological pinnacle and is no longer capable of changing.

That is the stark, controversial view of a group of biologists who believe a Western lifestyle now protects humanity from the forces that used to shape Homo sapiens.

'If you want to know what Utopia is like, just look around - this is it,' said Professor Steve Jones, of University College London, who is to present his argument at a Royal Society Edinburgh debate, 'Is Evolution Over?', next week. 'Things have simply stopped getting better, or worse, for our species.'

There is more, including quotes from Chris Stringer noting the continuing evolutionary change during the past 10,000 years. There seems to have been much emphasis on trying to predict where things are going in the future.

Then, there is this article by Freeman Dyson in New Perspectives Quaterly from this summer:

Now, after some 3 billion years, the Darwinian era is over. The epoch of species competition came to an end about 10,000 years ago when a single species, Homo sapiens, began to dominate and reorganize the biosphere. Since that time, cultural evolution has replaced biological evolution as the driving force of change. Cultural evolution is not Darwinian. Cultures spread by horizontal transfer of ideas more than by genetic inheritance. Cultural evolution is running a thousand times faster than Darwinian evolution, taking us into a new era of cultural interdependence that we call globalization. And now, in the last 30 years, Homo sapiens has revived the ancient pre-Darwinian practice of horizontal gene transfer, moving genes easily from microbes to plants and animals, blurring the boundaries between species. We are moving rapidly into the post-Darwinian era, when species will no longer exist, and the evolution of life will again be communal.

As he explains early in the essay, Dyson is building here on the ideas of Carl Woese, referring to early microbial evolution as "pre-Darwinian" because of the prevalence of horizontal gene transfer.

Well, there's surely no harm in watching more TV...

That's the story in this article by Patrizia Pernter and colleagues:

A possible cause of death of the Iceman -- a ca. 5,300 BP natural human glacier mummy from the Tyrolean Alps -- is an intrathoracic stone arrowhead. The aim of this study was to prove radiologically his enigmatic cause of death. In August 2005, the Iceman underwent his first multislice computed tomography examination. As the main pathologic finding, the left dorsal subclavian artery contures shows a 13 mm-long part where the vessel wall is damaged and a 3 mm-long irregular pseudo-aneurysm -- a typical complication of a laceration of the subclavian artery. In the surrounding soft tissue a large haematoma is visible. Historic records highlight the fatal destiny of subclavian artery injuries e.g. due to massive active bleeding and shock-related cardiac arrest. Therefore, the Iceman's cause of death by an arrowhead lacerating among others the left subclavian artery and leading to a deadly hemorrhagic shock can be now postulated with almost complete certainty, especially when taking the environmental (3,210 meters above sea level) and historic (5,300 BP) settings into account.

But did he have the lactase persistence allele?

References:

Pernter P, Gostner P, Vigl EE, Rühli FJ. 2007. Radiologic proof for the Iceman's cause of death (ca 5,300 BP). J Archaeol Sci (in press) doi:10.1016/j.jas.2006.12.019

The NY Times has an article by Sandra Blakeslee describing geological evidence for recent (i.e. Holocene) megatsunamis:

The explanation is obvious to some scientists. A large asteroid or comet, the kind that could kill a quarter of the world's population, smashed into the Indian Ocean 4,800 years ago, producing a tsunami at least 600 feet high, about 13 times as big as the one that inundated Indonesia nearly two years ago. The wave carried the huge deposits of sediment to land.

It's set up as an opposition between these geologists (notably, Dallas Abbott) and astronomers, who don't think there are enough big space rocks to cause that many recent impacts.

And of course there is the requisite mythical flood connection:

Dr. Masse analyzed 175 flood myths from around the world, and tried to relate them to known and accurately dated natural events like solar eclipses and volcanic eruptions. Among other evidence, he said, 14 flood myths specifically mention a full solar eclipse, which could have been the one that occurred in May 2807 B.C.

(via Gene Expression)

Wired has a short article by Annalee Newitz about recent evolutionary changes and their implications for futurists:

"I think my work is changing people's ideas about evolution, because now natural selection seems to have continued all the way up to the present day," said [Jonathan] Pritchard. "There's no reason to think it stops now."

That's why futurists like [Ray] Kurzweil are excited about Lahn and Pritchard's work -- it could lay the foundations for a new understanding of evolution that's more tolerant of the idea that humans should intervene in their own genetic transformation.

[Bruce] Lahn is comfortable with this idea. "If there's an evolutionary advantage to be had by using technology, then people will do it," he said. "People are going to start changing the game in evolution in ways Darwin never anticipated."

Trans-humanist pundit James Hughes, author of Citizen Cyborg, thinks it's time to speed up the evolutionary process.

"You can take what nature gave you, but there's no good reason to take nature as a guide for where you should go in the future," Hughes said.

Now, that's an angle I hadn't thought of, and I've been thinking about this a lot. But it does make sense -- there's nothing inviolate about being human in the way we are now, since humans keep on changing.

A new article in Science is claiming that the Easter Island population did not have a long duration on the island, and probably did not cause its own population crash.

There is a LiveScience news account by Ker Than, with some great quotes:

Lipo thinks the story of Easter Island's civilization being responsible for its own demise might better reflect the psychological baggage of our own society than the archeological evidence.

"It fits our 20th-century view of us as ecological monsters," Lipo said. "There's no doubt that we do terrible things ecologically, but we're passing that on to the past, which may not have actually been the case. To stick our plight onto them is unfair."

Ann Gibbons' Science news article on the paper is also pretty helpful.

[Terry] Hunt and co-author Carl Lipo of California State University, Long Beach, took eight samples of wood charcoal from the bottom of the oldest known archaeological site on the island, called Anakena. When they got radiocarbon dates that clustered at about 1200 C.E., Hunt at first assumed the dates were wrong and put them aside. But later he and Lipo decided to scrutinize all earlier dates from Anakena, to make sure they did not contain carbon from marine organisms or old wood, which can skew dates too old. After discarding what they considered unreliable dates, the pair found a high probability (50%) for the first human settlement starting just after 1200 C.E. The evidence does not rule out an occupation at 1000 C.E., but the probability is very low, says Hunt. The new dates are a "significant improvement" over the old ones, says radiocarbon-dating expert Tim Higham of Oxford University, U.K.

Although several researchers welcome the rigorous analysis of dates, not everyone agrees with the criteria the team used. "Some of his criteria are fair; others are not," says zoologist David Steadman of the Florida Museum of Natural History in Gainesville, whose 1000 C.E. dates for Anakena were left in the pair's analysis.

The new results are in keeping with a trend in the past decade toward later dates for colonization of some of the outermost Pacific islands. "This is an important paper, because it is part of a revision on the chronology of the Pacific that shows there is a big gap between settling west Polynesia [e.g., Samoa] and the marginal areas of south and east Polynesia," such as New Zealand, says archaeologist Atholl Anderson of the Australian National University in Canberra.

And then there were the rats. From LiveScience:

"The collapse was really a function of European disease being introduced," Lipo said. "The story that's been told about these populations going crazy and creating their own demise may just be simply an artifact of [Christian] missionaries telling stories."

At a scientific meeting last year, Hunt presented evidence that the island's rat population spiked to 20 million from the years 1200 to 1300. Rats had no predators on the island other than humans, and they would have made quick work of the island's palm seeds. After the trees were gone, the island's rat population dropped off to a mere 1 million.

Of course, the reason why this is a story is that it cuts against the Diamond collapse explanation.

Thinking about it, islands just aren't very good analogies for most human societies. A group of people get to an island; there's no disease that they didn't bring with them; there are plenty of animals and plants with no natural resistance to human predation. Humans can have a pretty high intrinsic growth rate under those circumstances -- 3 kids per women can take your group from 20 to 60,000 in 400 years.

Now what do you do? Malthusian dynamics are not our fault, especially when the rats get there first.

References:

Gibbons A. 2006. Dates revise Easter Island history. Science 311:1360. DOI link

Hunt TL, Lipo CP. 2006. Late colonization of Easter Island. Science (published online) Abstract

I was just taking notes on this paper by Sealy and Pfeiffer (2000), and found some good quotes about body size in the Bushmen, both historically and in archaeological samples:

Historical and ethnographic sources consistently indicate that Khoisan peoples were and continue to be petite. A group of early-20th-century San studied by Dart (1937a, b) had mean statures of 155.8 cm (males) and 146.1 cm (females). Decades later, the Harvard Kalahari study found mean statures of 160.9 cm (males) and 150 cm (females). These values are comparable to the fifth centile of adult stature for contemporary North Americans (Abraham 1979). Adult weights reported for the more recent individuals are 47.9 kg (males) and 40.1 kg (females) (Truswell and Hanson 1976).

It has been claimed that environmental stressors, especially shortages of food, affected growth (Dornan 1975:80; Almeida 1965:6). The secular trend towards increasing stature among mid-20th-century Khoisan (Tobias 1978) could be seen as evidence for the influence of environmental factors.

At the same time, there is a genetic component. Low stature persists even under apparently favourable health conditions. The small body size and lean physique of living Khoisan peoples are often cited in human population biology texts as exemplary of adaptation to a hot, sometimes specifically desert, climate. Their low body-mass index is portrayed as support for Bergmann's and Allen's rules (cf. Molnar 1998, Relethford 1997). Through study of archaeologically derived materials, these hypotheses can be explored.

That's on the historic record. They examine a number of skeletons from archaeological sites and report this:

Dimensions of selected bones from the southern Cape sample are summarized in table 2. Data from one exceptionally small skeleton (UCT 345, probably a dwarf) and the three most recent skeletons with anomalous isotope values (Sealy 1997) are not included in the summary statistics for body size. The mean stature calculated from 20 male femora is 157.8 cm (s.d. = 7.9). Twenty-three female femora have a mean estimated stature of 146.9 cm (s.d. = 10.5). Greater variability among females results from some very small individuals between 4,000 and 2,000 B.P. (see fig. 4). Body size, represented by femoral head diameter to maximize sample size and divided into five sex categories, is plotted against radiocarbon date in figure 5. This figure illustrates that the smallest individuals (femora < 375 mm, therefore < 139 cm tall; femoral head diameters < 34 mm) are "probable" females, classified as female only on the basis of body size and gracility. Hence it may be inappropriate to include them in the calculation of mean female stature. Excluding the four very petite probable females, mean female stature is 149.9 cm (s.d. = 8.5). The four smallest adults appear to be of normal proportions. Only eight males and five females are sufficiently complete for living body mass to be estimated, as this requires both femoral length and bi-iliac diameter. The estimated value is 42.8 ± 6.6 kg for males, 38.3 ± 4.4 kg for females.

That's 4'10'' for females; 5'2'' for males in the archaeological sample. Bi-iliac diameter for males was 214.6 ± 16.8, for females 209.0 ± 12.3.

Not much to do but link to this and wait for the paper to appear:

[Jean-Pierre] Bocquet-Appel and anthropology graduate student Stephan Naji analyzed skeletal remains in 62 prehistoric North American cemeteries.

They found that the number of immature skeletons increased by 37 percent over a 600-to-800 year period that coincides with the adoption of farming in North America about 2,500 years ago.

...

The baby-boom pattern has been observed in African and European cemeteries dating about 5,000 to 7,000 years earlier, according to Bocquet-Appel. This period also coincides with the shift in those regions from foraging to agriculture at the end of the Stone Age.

It's hard to beat the abstract of this paper by Eric Wang and colleagues (2006):

By using the 1.6 million single-nucleotide polymorphism (SNP) genotype data set from Perlegen Sciences [Hinds, D. A., Stuve, L. L., Nilsen, G. B., Halperin, E., Eskin, E., Ballinger, D. G., Frazer, K. A. & Cox, D. R. (2005) Science 307, 1072-1079], a probabilistic search for the landscape exhibited by positive Darwinian selection was conducted. By sorting each high-frequency allele by homozygosity, we search for the expected decay of adjacent SNP linkage disequilibrium (LD) at recently selected alleles, eliminating the need for inferring haplotype. We designate this approach the LD decay (LDD) test. By these criteria, 1.6% of Perlegen SNPs were found to exhibit the genetic architecture of selection. These results were confirmed on an independently generated data set of 1.0 million SNP genotypes (International Human Haplotype Map Phase I freeze). Simulation studies indicate that the LDD test, at the megabase scale used, effectively distinguishes selection from other causes of extensive LD, such as inversions, population bottlenecks, and admixture. The 1,800 genes identified by the LDD test were clustered according to Gene Ontology (GO) categories. Based on overrepresentation analysis, several predominant biological themes are common in these selected alleles, including host-pathogen interactions, reproduction, DNA metabolism/cell cycle, protein metabolism, and neuronal function.

Most tests of selection are blunt instruments. They depend on observations of the frequency spectrum of mutations, but mutations don't happen very often for most genetic loci. With most methods, recent selection is very difficult to find. It's like trying to find potholes when you're driving a tank -- it takes a pretty big pothole to notice anything. To find a higher proportion of the selection that happened, you need a more sensitive metric.

The mark of a selected allele is a rapid increase in frequency. If the selection is recent, then the allele should have appear to originate recently. A rapid increase in the frequency of an allele leaves a pattern of linkage disequilibrium (LD), because recombination does not have a chance to break the selected locus apart from nearby neutral loci. The longer ago the allele increased in frequency, the more recombination and the less LD.

Wang et al. (2006) used the prediction that the LD should decrease over time to establish a test of recent selection. They surveyed the linkage among nearby SNPs to determine whether a variant has increased rapidly in frequency during the recent past. The sensitivity of this test depends on the SNP coverage of the genome. At present, SNP coverage is very good for variants with moderate to high frequencies, so although low-frequency selected variants (those with less than a 5 - 10 percent global frequency) were missed by the current survey, it has found a huge number of selected loci.

In conclusion, we have introduced a simple probabilistic method to detect unusual genetic architectures associated with recent selection that does not require haplotype information. It is, therefore, suitable for large chromosomal scans with large population samples. Homo sapiens have undoubtedly undergone strong recent selection for many different phenotypes, including but certainly not limited to the general categories we have defined in this work (Fig. 5). Such inferred selective events are not rare (Fig. 3). The numbers obtained, however, are similar to estimated numbers obtained for artificial selection (by humans) on the maize genome (45). Given that most of these selective events likely occurred in the last 10,000 Ð 40,000 years, a time of major population expansion out of Africa followed by regional shifts from hunterÐgatherer to agrarian societies, it is tempting to speculate that gene Ð culture interactions directly or indirectly shaped our genomic architecture (46, 47). As such, we suggest that such recently selected alleles may provide
useful "markers" for investigating the evolutionary migrations of our species, as an adjunct to studies using neutral markers. We also propose that many of these alleles, because of their high prevalence and recent selection, should be considered likely "functional candidates" for association with human variability and the common disorders afflicting humankind.

They also assign the loci with evidence of recent selection to different functional categories. Pathogen-host interaction loci have a high representation in the recently selected genes, as do genes related to protein and gene metabolism. And this:

One of the more intriguing categories overrepresented in inferred selective events is neuronal function. We define this category to include a diverse assortment of genes, including the serotonin transporter (SLC6A4), glutamate and glycine receptors (GRM3, GRM1, and GLRA2), olfactor y receptors (OR4C13 and OR2B6), synapse-associated proteins (RAPSN), and a number of brain-expressed genes with largely unknown function (ASPM, RNT1; see Fig. 4).

It would be hard for me to overstate how important this paper is. Even if it weren't central to my own current research (about which you will just have to wait for more), it brings home the vast importance of adaptive change during the most recent parts of human evolution.

References:

Wang ET, Kodama G, Baldi P, Moyzis RK. 2006. Global landscape of recent inferred Darwinian selection for Homo sapiens. Proc Nat Acad Sci USA 103:135-140. Abstract

Jared Diamond has a short review article in Nature on the evolution of skin color. This is an old story in anthropology, but it has taken some interesting twists lately with the assessment of genetic variability in some of the genes related to pigmentation. This short review covers recent papers by Nina Jablonski (2004) and George Chaplin (2004). After a short history of how skin reflectance has been measured, Diamond cuts to the selective point:

Jablonski and Chaplin prefer a combination of two selective factors involving several costs and one benefit of UVR [ultraviolet radiation]. The costs involve the destructive photolysis of many compounds, of which Jablonski and Chaplin attach particular importance to the B vitamin folate. Everybody requires folate, so everybody would have dark skins (to screen out UVR and reduce photolysis) if there were no other selective factors. However, UVR also provides a benefit: catalysing the synthesis of vitamin D. Hence skin colour evolves as a compromise between skins light enough to permit UVR penetration for vitamin D synthesis, but dark enough to reduce folate photolysis (283).

The folate explanation is probably the most distinctive aspect of Jablonski and Chaplin's take on skin coloration, and Diamond naturally wonders what happened to the hypothesis that skin cancer was a primary selective factor:

Although the harmful effects of UVR are often taken to be especially associated with skin cancer, Jablonski and Chaplin minimize the importance of this aspect on the grounds of the late age of onset, after some or most of a couple's children have been morn. Most geneticists similarly minimize the selective importance of damage or disease late in life.

Here I am sceptical. This common view may be valid for mammal species in which parent-offspring ties are severed soon after weaning, but it overlooks three of the most distinctive features of human life-histories in traditional societies: the long post-weaning dependence of offspring on parents for learning and then for social status, the large contribution of hunter-gatherer grandmothers to their grandchildren's food supply, and the dependence of an entire band or village on its oldest people as the repositories of knowledge in a preliterate society. It would be interesting to try to estimate the selective importance of skin cancers for skin-colour evolution from this perspective... (283).

Before my reaction, it should be noted that the great importance of folate in the hypothesis of Jablonski and Chaplin is also a distinctive character of our species. Since folate is of paramount importance for normal neural growth during fetal development, the uniquely large and complex brains of humans are a greater target of selection to avoid folate photolysis.

But Diamond's objection about skin cancer is also interesting in light of recent genomic findings concerning targets of positive selection in human evolution. Nielsen et al. (2005) (reviewed in a previous post) found that several of the genes showing the strongest evidence for positive selection in the human lineage were related to cancer risk.

I think it likely that these genes are positively selected in order to reduce cancer risk in humans, because of our uniquely long lifespans compared to most primates, and because of the great importance of older individuals to the survival and reproduction of their younger kin. It is possible that some of these genes are particularly selected because of skin cancer itself, since the human adaptation to resist skin cancer must have been initiated as hominids lost their body fur. This time was likely substantially earlier than either any great increase in longevity or any great increase in the importance of older adults. For this reason, skin cancer risk may have been one of the earliest factors leading to selection on genes associated with tumor growth and other aspects of cancer etiology.

Diamond also discusses exceptions to the pattern of correlation of skin color with UVR intensity:

Of the 12 most negative residuals (skins unexpectedly dark), the highest and four others are for Bantu-speaking southern African populations that migrated from the Equator towards high southern latitudes only 2000 years ago. These populations have not yet had enough time for evolutionary loss of their equatorially adapted dark skins. Conversely, three of the nine most positive residuals (skins unexpectedly pale) are for peoples of the Philippines, Vietnam and Cambodia, who migrated towards the equator from high latitudes only in recent millennia and have not yet evolved appropriately dark skins. But why do the people of Bougainville Island in the South Pacific, and why did the Aboriginal Tasmanians, have such dark skins, after more than 10,000 years of in situ adaptation? (284)

An answer to this question might be found in the nature of genetic alterations that lead to pigmentation levels in humans. Diamond's short review does not discuss this research, but an entrée may be found in an article on MC1R variation by Harding et al. (2000). The structure of global variation in this gene shows a relatively low level of allelic diversity in Africans and a higher level outside of Africa. The Eurasian population in particular has a high number of unrelated alleles, with many of the alleles functionally related to lighter skin tones and hair colors. The apparent pattern for this gene is a strong selective constraint within Africa for a functionally dark pigmentation, with a contrasting pattern outside Africa. This contrast may be based on a relative relaxation of selection at higher latitudes, or conversely it may reflect positive selection for many different mutations, all of which result in lighter skin color. In either case, the striking aspect of the pattern is the many ways in which skin color may be light, corresponding to the spread of several distinct mutations in the non-African human population.

When considering small island populations, a natural hypothesis is that the necessary mutations to lighten skin color were rare enough that they may not have occurred. But the range of different mutations effectively resulting in lighter skin (if the variation of MC1R may provide a model for at least some of the genes related to skin color) tends to make me think that adaptive mutations (resulting in lighter skin) were not unlikely. For this reason, I think we must turn to the level of selection on skin color, which was either absolutely low in these populations or relatively low compared to the rate of genetic drift.

So Diamond's question is an important one, because it essentially asks why selection upon skin color should be high in some populations and low in others. This variable nature of selection in different human populations is a venue in which we may see many more similar questions in the future.

References:

Chaplin G. 2004. Geographic distribution of environmental factors influencing human skin coloration. Am J Phys Anthropol 125:292-302. PubMed

Diamond J. 2005. Geography and skin color. Nature 435:283-284. Nature online

Harding RM et al. 2000. Evidence for variable selective pressures at MC1R. Am J Hum Genet 66:1351-1361.

Jablonski N. 2004. The evolution of human skin and skin color. Annu Rev Anthropol 33:585-623.

Nielsen R, et al.. 2005. A Scan for Positively Selected Genes in the Genomes of Humans and Chimpanzees. PLoS Biol 3:e170. PLoS Online

There is a very nice review paper with that title in the American Journal of Clinical Nutrition, by Loren Cordain and colleagues. The basic story is in the first two sentences of the abstract:

There is growing awareness that the profound changes in the environment (e.g., in diet and other lifestyle conditions) that becan with the introduction of agriculture and animal husbandry ~10 000 y ago occurred too recently on an evolutionary time scale for the human genome to adjust. In conjunction with the discordance between our ancient, genetically determined biology and the nutritional, cultural, and activity patterns of contemporary Western populations, many of the so-called diseases of civilization have emerged (341).

This is far from a new story; it is what I have taught in my 100-level courses for a long time. But there are some great facts and statistics in the paper that make it a good resource.

For example, did you know:

Taken together, the addition of manufactured salt to the food supply and the displacement of traditional potassium-rich foods by foods introduced during the Neolithic and Industrial periods caused a 400% decline in the potassium intake while simultaneously initiating a 400% increase in sodium ingestion (350).

Although the article introduces the issue by contrasting the putative hunter-gatherer diet with the Western diet, much of its concrete illustrations derive from the industrial revolution. The article tends to conflate these as in the above quote, and it would be worthwhile to separate these effects a bit more (although difficult because the probable degree of malnutrition and nutrient deficiency inherent in the early agricultural diet contrasts with the nutritional excesses of the Western diet.

Here's another one:

The typical Western diet yields a net acid load estimated to be 50 mEq/d. As a result, healthy adults consumed the standard US diet sustain a chronic, low-grade pathogenetic metabolic acidoses that worsens with age as kidney function declines. Virtually all preagricultural diets were net base yielding because of the absence of cereals and energy-dense, nutrient-poor foods -- foods that were introduced during the Neolithic and Industrial Eras and that displaced base-yielding fruit and vegetables (350).

The main parts include a review of the advent of new foods, including dairy, cereals, refined sugars, oils, alcohol, salt, and domesticated meats, and some of the health consequences of those changes.

References:

Cordain L, Eaton SB, Sebastian A, Mann N, Lindeberg S, Watkins BA, O'Keefe JH, and Brand-Miller J. 2005. Origins and evolution of the Western diet: health implications for the 21st century. Am J Clin Nut 81:341-354.