Early European mtDNA: only mysterious if you want it to be

A paper by Wolfgang Haak and colleagues in this week's Science sequenced ancient mtDNA in 24 Neolithic European skeletons.

A review by Martin Richards (2003) lays out the genetic evidence about population dynamics in Neolithic Europe, along with the likely scenarios. I recommend the paper, it clarified matters for me. During the past thirty years, Cavalli-Sforza and others have pushed a model called "demic diffusion" for Neolithic Europe -- essentially the idea that population growth resulted in the net movement of Near Eastern genes across Europe. But there are other models for population interactions as agriculture spread and populations became more dense -- including long-distance colonizations, elite dominance by one group or another, cultural diffusion without significant genetic movement, and so on.

The main question recently has been about the strength of net movement of genes into Europe. Some have claimed that the majority of present European genes can be traced to the Near East before 6000 years ago. Others have argued that the genetic influence of West Asian populations was substantially more minor, or at least had extended over a longer time from the Upper Paleolithic to the present, instead of being concentrated in the Neolithic revolution itself.

The current paper places itself in the frame of this ongoing debate, but raises an entirely new problem! The abstract:

The ancestry of modern Europeans is a subject of debate among geneticists, archaeologists, and anthropologists. A crucial question is the extent to which Europeans are descended from the first European farmers in the Neolithic Age 7500 years ago or from Paleolithic hunter-gatherers who were present in Europe since 40,000 years ago. Here we present an analysis of ancient DNA from early European farmers. We successfully extracted and sequenced intact stretches of maternally inherited mitochondrial DNA (mtDNA) from 24 out of 57 Neolithic skeletons from various locations in Germany, Austria, and Hungary. We found that 25% of the Neolithic farmers had one characteristic mtDNA type and that this type formerly was widespread among Neolithic farmers in Central Europe. Europeans today have a 150-times lower frequency (0.2%) of this mtDNA type, revealing that these first Neolithic farmers did not have a strong genetic influence on modern European female lineages. Our finding lends weight to a proposed Paleolithic ancestry for modern Europeans (Haak et al. 2005:1016).

Some observations:

1. This is the latest in a long line of ancient DNA results that depends on the strangeness of the observation to argue against contamination.

The observed distinct N1a types rule out the possibility of contamination with modern samples, which can be a problem in ancient human DNA studies. It is implausible that the five types are from five different modern contaminants, because the frequency of this type today is very low anywhere in the world, at about 0.2% (2325) (fig. S1). It is also unlikely that the sequence variations seen within the five N1a types are the result of random postmortem DNA damage (26, 27), because three out of six sequence types that we have identified precisely match modern sequences previously published in the literature (table S2 and supporting references); finally, two further N1a types (HAL2 and UWS5) precisely fit into predicted but previously unobserved ancestral nodes in the N1a phylogeny (Fig. 2), underlining the authenticity of the ancient DNA.

It may be that there is just nothing else to be done, but it is troublesome from the perspective of hypothesis testing. Will we ever see a paper that says "ancient DNA demonstrates perfectly ordinary sequences in prehistoric people"? OK, I guess Caramelli et al. (2003) (which reported modern mtDNA sequences in some Upper Paleolithic Italian specimens) had that theme, but I have heard many people question that result for this precise reason.

2. The pattern here is a remarkable echo of the Neandertal mtDNA problem. Here we have a common variant in Europe only 7500 years ago that today is almost gone. With the Neandertals, we have a very common variant that today, after 40,000 years, is completely gone.

You might therefore expect that some clever geneticists would claim that the Neolithic farmers contributed little or no genetic ancestry to living Europeans. And that is precisely the hypothesis discussed by Haak et al. (2005):

These simulations reject the simple hypothesis in which modern Europeans are direct descendants of these first farmers and have lost N1a mainly by genetic drift. Hence the simulations confirm that the first farmers in Central Europe had limited success in leaving a genetic mark on the female lineages of modern Europeans. This is in contrast to the success of the Neolithic farming culture itself, which subsequently spread all over Europe, as the archaeological record demonstrates. One possible explanation is that the farming culture itself spread without the people originally carrying these ideas. This includes the possibility that small pioneer groups carried farming into new areas of Europe, and that once the technique had taken root, the surrounding hunter-gatherers adopted the new culture and then outnumbered the original farmers, diluting their N1a frequency to the low modern value. Archaeological research along the Western periphery of LBK and isotope studies of some of our sampled individuals seem to support the idea that male and female hunter-gatherers were integrated into the Neolithic communities (3, 10, 29). This hypothesis implies that N1a was rare or absent in Mesolithic Europeans, which may be a reasonable assumption given the rarity of the N1a type anywhere in the world (Fig. 3). An alternative hypothesis is a subsequent postearly-Neolithic population replacement in Europe, eliminating most of the N1a types. Archaeological evidence for such an event is as yet scant (Haak et al. 2005:1018).

Of course, this idea depends on several unknowns. It proposes that European hunter-gatherers who were contemporary with the LBK culture had very different mtDNA types -- indeed, that they had the types that are presently common. And it proposes that the intrinsic growth rate of agriculturalists was very small, so that their genes were flooded by hunter-gatherers transitioning to agriculture.

But if their genes were so flooded at every stage of their expansion, then the N1a mtDNA sequences shouldn't be there in the first place -- they should have been left behind in the Near East. So this is a very curious event -- an expanding population saw one of its major mtDNA variants greatly contract in frequency, so much so that today it is nearly gone.

3. Let's review the facts. The mysterious N1a mtDNA type is currently rare anywhere in the world. It is carried by only 0.2 percent of Europeans. But it has a high frequency among these Neolithic Europeans -- 25 percent of the samples, which means the true population frequency was likely between 8 and 42 percent (Haak et al. 2005:1017). The paper found that this great reduction in frequency within Europe cannot have been accomplished by genetic drift.

Can someone tell me why the word "selection" doesn't appear in this paper?

References:

Balter M. 2005. Ancient DNA yields clues to the puzzle of European origins. Science 310:964-965. Full text (subscription)

Haak W et al. 2005. Ancient DNA from the first European farmers in 7500-year-old Neolithic sites. Science 310:1016-1018. Full text (subscription)

Richards M. 2003. The Neolithic invasion of Europe. Annu Rev Anthropol 32:135-162. Full text