population growth

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

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

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

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

Endocranial volume against time for fossil Homo.

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

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

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

It just didn't happen.

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

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

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

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

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

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

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

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

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

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

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

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

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

References:

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

The cover story in Nature this week is a paper about the population history of India, from David Reich's lab. It's an important contribution to our knowledge of human genetic variation, and provides a very interesting set of data for further investigation of modern human origins, the dispersal of agriculture into the subcontinent, and the history of more recent Indian populations.

Here's the abstract:

India has been underrepresented in genome-wide surveys of human variation. We analyse 25 diverse groups in India to provide strong evidence for two ancient populations, genetically divergent, that are ancestral to most Indians today. One, the 'Ancestral North Indians' (ANI), is genetically close to Middle Easterners, Central Asians, and Europeans, whereas the other, the 'Ancestral South Indians' (ASI), is as distinct from ANI and East Asians as they are from each other. By introducing methods that can estimate ancestry without accurate ancestral populations, we show that ANI ancestry ranges from 39–71% in most Indian groups, and is higher in traditionally upper caste and Indo-European speakers. Groups with only ASI ancestry may no longer exist in mainland India. However, the indigenous Andaman Islanders are unique in being ASI-related groups without ANI ancestry. Allele frequency differences between groups in India are larger than in Europe, reflecting strong founder effects whose signatures have been maintained for thousands of years owing to endogamy. We therefore predict that there will be an excess of recessive diseases in India, which should be possible to screen and map genetically.

The number of individuals is not huge for the purposes of population genetic analysis -- only 132 people from 25 groups -- but it is very significant in terms of recent samples. By comparison, it is around double the number of effective individuals in any of the HapMap v.1 populations, genotyped at more than 560,000 SNPs.

The results of the study are basic population genetic issues, including the degree of endogamy, the pattern of regional differentiation, the likelihood of discovering new recessive genetic disorders by additional sampling. Some notes:

Population mixture. The authors propose that today's groups descend in varying proportions from two ancient (and no longer existing) populations, which they call "ancestral North Indian" and "ancestral South Indian".

I'm always skeptical of mixture models, especially when the putative source populations no longer exist. There are just too many ways that structured migration or dispersal can lead to the appearance of mixture. People once thought of "Alpines" as a mixture of pure Nordic and Mediterranean elements, after all-- and that was just because their heads were mesocephalic.

Still, with a half-million SNPs, it's possible to do a better job testing the hypothesis of mixture versus structured migration. The authors in this paper didn't -- they applied a simplified "3 Population Test" that compares the empirical allele frequencies to proportions expected under only two scenarios: simple mixture or complete isolation. It seems to me that the null should be simple isolation by distance, which would give the same result as "mixture" according to their test. If you really want to look for population mixture, you need to involve the dimension of time, for example, by demonstrating the antiquity of haplotypes that have mixed together.

So I don't accept this ancestral division, certainly not at face value. It does seem plausible that West Asian (and thereby European-related) genes have introgressed into India over time, perhaps in association with the growth of high-density agricultural populations. Maybe some of this gene flow occurred under the influence of positive selection, but processes of elite dominance and differential growth may have been sufficient.

Regional differences. The results show a greater degree of regional genetic differentiation in India than has been found for continental Europe. Still, with an F_ST of only 0.01, we're not talking about major population splits here. With that number, the subcontinent is closer to panmixia than one might expect for a region its size. The authors suggest that founder effects explain the regional differentiation:

We propose that the high FST among Indian groups could be explained if many groups were founded by a few individuals, followed by limited gene flow. This hypothesis predicts that within groups, pairs of individuals will tend to have substantial stretches of the genome in which they share at least one allele at each SNP. We find signals of excess allele sharing in many groups (Supplementary Fig. 2), which as expected tend to occur in the groups that have the highest FST values from all others (P = 0.002 for a correlation). To estimate the age of founder events, we measured the genetic distance scale over which allele-sharing decays, and verified the robustness of our procedure by simulation (Supplementary Fig. 3). Six Indo-European- and Dravidian-speaking groups have evidence of founder events dating to more than 30 generations ago (Supplementary Fig. 2), including the Vysya at more than 100 generations ago (Fig. 2). Strong endogamy must have applied since then (average gene flow less than 1 in 30 per generation) to prevent the genetic signatures of founder events from being erased by gene flow.

I don't think that explanation works. With those times in generations, we're talking about events within the last 600-2000 years. Since all these calculations are done on the whole dataset assuming complete neutrality, I think we should look more closely at the distribution of LD across loci. It seems likely that some of the high-LD loci that appear to point to founder effects will actually be found to be selected.

Relationships of Indian to non-Indian populations. One of the real problems of assuming a tree with no migration is that it leads to statements like this:

[T]he ANI [ancestral North Indian] and CEU [HapMap European sample] form a clade, and further analysis shows that the Adygei, a Caucasian group, are an outgroup (Supplementary Note 4). Many Indian and European groups speak Indo-European languages, whereas the Adygei speak a Northwest Caucasian language. It is tempting to assume that the population ancestral to ANI and CEU spoke 'Proto-Indo-European', which has been reconstructed as ancestral to both Sanskrit and European languages, although we cannot be certain without a date for ANI–ASI mixture.

Some of the common ancestors of some living Europeans and some Indians were probably speakers of proto-Indo-European speakers. But we can easily refute the hypothesis that all of the common ancestors did so -- some of those common ancestors lived more than 40,000 years ago, as is well-known from the mtDNA chronology. The tree model with complete isolation does not explain the data. So as simple as it is -- and as well-used by Cavalli-Sforza and others -- it would be better to use a more accurate model.

UPDATE (2009-09-24): Gene Expression has a full review of the paper.

UPDATE (2009-09-27): Very interesting angle by Suvrat Kher at Reporting on a Revolution:

The Indian Press has made a hash of the finding....

But I can't blame the press entirely. The scientists who gave interviews to the press didn't mention this. They wimped out on reporting this potential inflammatory and politically incorrect finding. This is just poor and irresponsible science outreach on part of the scientists. How can you ignore a finding that is staring out at you from the very paper you are talking about? The press may be guilty of not digging in but it was just reporting what the scientists told them.

References:

Reich D, Thangaraj K, Patterson N, Price AL, Singh L. 2009. Reconstructing Indian population history. Nature 461:489-494. doi:10.1038/nature08365

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