In my comments on the recent Hammer et al. paper on Africa, I noted that the naive Out of Africa edifice has been shattered by recent discoveries, and attempts to patch it up by postulating a little admixture here, a little admixture there are largely unconvincing. We need a radically new model, so it was a nice surprise for me to see a new paper that attempts to do just that in a quantitative manner.
Currat & Excoffier address two of the holes of the current working model:
- Why Chinese don't have less Neandertal admixture than Europeans, even though Neandertals were a West Eurasian distributed species
- Why no Neandertal mtDNA is detected in modern samples
This is contradicted by another recent study by Ghirotto et al. focused entirely on the problem of Neandertal mtDNA (non)-intogression. I tend to side with G. et al. on this issue, as we currently have not only 100-strong samples from around the world, but, literally, tens of thousands of mtDNA samples, and perhaps even more if we account for commercial testing: no Neandertal sequences have turned up. So, I don't think it's the case that Neandertal mtDNA admixture is so low that we're not finding it in small (100-strong) samples.
We thus simulated the genealogy of 20 samples of 100-mtDNA sequences scattered over all Eurasia, and we estimated the fraction of these current lineages to be of Neanderthal ancestry by using a conservative interbreeding success of 2% for the hybrids. Among 10,000 simulations of this process, we could never observe any mitochondrial sequence of Neanderthal origin in our samples. We thus conclude that an interbreeding success smaller than 2% for Neanderthal-human hybrids is fully compatible with limited Neanderthal nuclear introgression and with no introgression of mtDNA.
In any case, the current paper's major contribution is tackling the problem of the equidistribution of Neandertal admixture across Eurasia, despite the fact that Neandertal was a West Eurasian distributed species.
The solution is simple: extend the Neandertal range eastwards, all the way to the Altai. That way, there is no mystery why French and Chinese have the same degree of Neandertal admixture: the former picked it up en route to France, the latter in their eastward journey to China. The extension of the Neandertal range to the east is supported by the close relationship of the Denisovan genome to Neandertals as well as the Okladnikov sample from Uzbekistan, so it is not simply a kludge, but a reasonably well-supported position.
I remain unconvinced for a variety of reasons:
- The extension of the Neandertal range works only if we assume that the Chinese ended up in China largely via an inner Asian route, rather than a coastal migration that has garnered increasing support from analyses of mtDNA and Y-chromosomes
- Moreover, even if the ancestors of the Chinese did follow a route via the heartland of Eurasia, that would not explain why south Eurasians would also possess the same levels of Neandertal admixture; that would require that not only East Eurasians, but also Australo-Melanesians and "Ancestral South Indians" to follow an inner Asian route that would bring them in protracted contact with Neandertals
- The expansion model also sidesteps the big elephant in the room: the fact that modern peoples are not necessarily descended primarily from the early modern humans who lived in the same localities as themselves. Neolithic and post-Neolithic events are increasingly thought to have shaped gene pools, so it is not clear, for example, to what extent the modern French are descended from Upper Paleolithic Europeans who ended up in France at the time when Neandertals were still in existence, and thus had the opportunity to mate with them along their route.
With respect to point #1, the authors write:
Although we have modeled the Asian range to extend up to the Altai region north of the Himalayas, we cannot be certain that the ancestors of East Asians migrated through this region. However, the facts that Papua New Guineans show signals of hybridization with another hominin (Denisovan) (2) and that their ancestors are likely to have followed a coastal southern route to the Pacific (19, 20) suggest that the Denisovan range must have extended more to the south and that the ancestors of East Asians may have indeed traveled north of the Himalayas, above the Denisovan range.
A northward migration route for East Asians and a southward one for Australo-Melanesians would solve the problem of "why Chinese are as Neandertal-admixed as the French" but would create a new problem of "why Papuans are also as Neandertal-admixed as the French", unless we derive everybody from the Altai.
The authors write:
Under our model of hybridization during range expansions, similar amounts of Neanderthal ancestry in France and China (Fig. S2) are more often observed if the geographical range of Neanderthals extended up to the Altai Mountains north of the Himalayas. Indeed, a hybridization range restricted to Europe, the Middle East, and the Caucasus region (including the brown and green areas in Fig. 1) would always lead to a much larger Neanderthal introgression level in Europe than in China (Figs. S2 and S3, light bars).It is important to note the differences between this model and the one in the Reich et al. and Green et al. papers from last year; the latter postulated a brief, but relatively intense episode of admixture in West Asia, and the subsequent colonization of the world by (slightly Neandertal-admixed) modern humans with minimal subsequent admixture.
The Currat & Excoffier favored model, on the other hand, posits exceptionally low admixture rates (or mostly infertile hybrids) but with repeating admixture events across a large geographical range that is extended far to the east.
I am not very supportive of either model:
- R&G can't convincingly explain why modern West Eurasians have the same amount of Neandertal "admixture" as every other Eurasian. They inhabited the same space as Neandertal for tens of thousands of years and had maximal opportunities to admix with them
- C&E save the phenomena by postulating an eastward Neandertal population, but it is not clear to me how relevant the inner Asian route was to the peopling of Asia as a whole
Hopefully, next year, we will see even more realistic simulation studies that include the second elephant in the room, archaic admixture in Africans. The discovery that Africans possess a degree of archaic African admixture from Homo populations that branched off before the split of modern humans and Neandertals leads to the inevitable conclusion that Eurasians (who lack this archaic African admixture) would appear closer to Neandertals based on the D-statistic used by R&G.
Happy were the days when human evolution could be viewed as a simple tree branching process, but now we have at least four players in the field (modern humans, Neandertals, Denisovans, archaic Africans) and we are bound to have new full ancient H. sapiens genomes. Things are bound to get more interesting.
Laurent Excoffier wrote to me in an e-mail:
Hi Dienekes,I've read your blog and liked your quite balanced discussion. However I havetwo comments on your main concerns:1) You seem to conclude that our model assumes that Chinese only followed anorthern route, but what we portray in our Figure 3 is a map representingintrogression event densities, which does not necessarily represent themigrations followed by the ancestors of Chinese people. In our simulations,migrants could indeed go South of the Himalaya, but since we assumed therewere no Neanderthals there, no admixture events occurred in this region. So,our model does not strictly assume a main northern migration route to Asia,but rather a concentric migration both North and South of the Himalayas,with some later secondary contacts in Eastern Asia.An important message of our paper is to say that whatever the migrationroutes to Asia, Asian populations having interacted with Neanderthals forabout the same amount of time (or in space) would have about the same finallevel of introgression. So we would not (and never did) say that East Asianhave followed a migration route North of the Himalayas.2) Concerning you big elephant, we indeed believe that current Europeans aremainly descending from Paleolithic people, and we have a specific paper onthis (Currat M, Excoffier L (2005) The effect of the Neolithic expansion onEuropean molecular diversity. Proceedings of the Royal Society London B 272,679-688), and a later paper examining and explaining why local genes are likelyto massively introgress the genome of populations invading the territory ofa local species (Currat M, Ruedi M, Petit RJ, Excoffier L (2008) Thehidden side of invasions: Massive introgression by local genes. Evolution62, 1908-1920). It thus appears very likely to us that the Paleolithic genepool of Europeans has largely persisted in modern humans, despite posteriorNeolithic migrations, if we assume that Neolithic populations mixed to someappreciable extent with local paleolithics during their expansion overEurope.Anyway, it is good that our paper promotes discussions on the dynamics ofthe settlement, and that spatial aspects of human evolution are now givensome importance.bestlaurent
With respect to point #1, I acknowledge that the C&E model does not explicitly choose either a northern or southern migration route for the ancestors of the Chinese. However, I do believe that it effectively chooses a mainly northern route. This is a simple consequence of geometry: concentric radiation of migrants results in more migrants flowing through the larger volume of the interior of the Eurasian continent (where they would have the opportunity to admix with eastern Neandertals) rather than through the narrower coastal band (where they would not).
It is also an interesting question whether the concentric model would lead to non-distinguishable admixture levels in East Asians and Australo-Melanesians, since -under the concentric migration model- the latter would mostly travel through regions of low-to-non-existent Neandertal occupation, whereas the former would not.
With respect to point #2, it is of course a hotly debated issue whether modern Europeans are largely descended from Paleolithic, Neolithic, or even post-Neolithic migrants. My reasons for preferring a more recent ancestry are:
The issue can only be settled, of course, if we are ever lucky enough to obtain ancient DNA from Upper Paleolithic Europeans.
- First, the published ancient DNA work, which showed a chasm between Mesolithic and modern mtDNA in central Europe, and seemingly non-existence of the main current European Y-haplogroup R1 in both Central Europe and France Neolithic sites (Treilles).
- Second, the observation of Fst values between European and West Asian populations are approximately 1/3 of those between West and East Eurasians. If the separation between Europeans and West Asians was effected close to the time of the Upper Paleolithic colonization of Europe (40ky), and would thus have diverged genetically only slightly less than West Eurasians and East Asians have.
PNAS doi: 10.1073/pnas.1107450108
Strong reproductive isolation between humans and Neanderthals inferred from observed patterns of introgression
Mathias Currat, and Laurent Excoffier
Recent studies have revealed that 2–3% of the genome of non-Africans might come from Neanderthals, suggesting a more complex scenario of modern human evolution than previously anticipated. In this paper, we use a model of admixture during a spatial expansion to study the hybridization of Neanderthals with modern humans during their spread out of Africa. We find that observed low levels of Neanderthal ancestry in Eurasians are compatible with a very low rate of interbreeding (<2%), potentially attributable to a very strong avoidance of interspecific matings, a low fitness of hybrids, or both. These results suggesting the presence of very effective barriers to gene flow between the two species are robust to uncertainties about the exact demography of the Paleolithic populations, and they are also found to be compatible with the observed lack of mtDNA introgression. Our model additionally suggests that similarly low levels of introgression in Europe and Asia may result from distinct admixture events having occurred beyond the Middle East, after the split of Europeans and Asians. This hypothesis could be tested because it predicts that different components of Neanderthal ancestry should be present in Europeans and in Asians.