Taiwanese mtDNA and the origins of Oceanic populations

I lectured about the origins of Polynesian populations in my genetics class today, and after class I noticed this new paper by Jean Trajaut and colleagues (Mackay Memorial Hospital, Taipei) in PLoS Biology. Here's the abstract:

Genetic affinities between aboriginal Taiwanese and populations from Oceania and Southeast Asia have previously been explored through analyses of mitochondrial DNA (mtDNA), Y chromosomal DNA, and human leukocyte antigen loci. Recent genetic studies have supported the ''slow boat'' and ''entangled bank'' models according to which the Polynesian migration can be seen as an expansion from Melanesia without any major direct genetic thread leading back to its initiation from Taiwan. We assessed mtDNA variation in 640 individuals from nine tribes of the central mountain ranges and east coast regions of Taiwan. In contrast to the Han populations, the tribes showed a low frequency of haplogroups D4 and G, and an absence of haplogroups A, C, Z, M9, and M10. Also, more than 85% of the maternal lineages were nested within haplogroups B4, B5a, F1a, F3b, E, and M7. Although indicating a common origin of the populations of insular Southeast Asia and Oceania, most mtDNA lineages in Taiwanese aboriginal populations are grouped separately from those found in China and the Taiwan general (Han) population, suggesting a prevalence in the Taiwanese aboriginal gene pool of its initial late Pleistocene settlers. Interestingly, from complete mtDNA sequencing information, most B4a lineages were associated with three coding region substitutions, defining a new subclade, B4a1a, that endorses the origin of Polynesian migration from Taiwan. Coalescence times of B4a1a were 13.2 3.8 thousand years (or 9.3 2.5 thousand years in Papuans and Polynesians). Considering the lack of a common specific Y chromosomal element shared by the Taiwanese aboriginals and Polynesians, the mtDNA evidence provided here is also consistent with the suggestion that the proto-Oceanic societies would have been mainly matrilocal.

In a few words, the backstory is that linguistic evidence suggested an expansion of Austronesian-speaking peoples out of South China or Taiwan, because the most ancient branches of the Australasia languages are now found only on Taiwan. But genetic evidence so far has been against this hypothesis, sometimes called the "express train" model because it predicts a rapid spread of agriculturalists through Indonesia and on to Polynesia. That evidence has consisted of surveys of mtDNA and Y chromosomes throughout Polynesia and island Southeast Asia, which have shown that the lineages most common in Polynesians do not occur in populations west or north of Java. Based on this kind of evidence and some archaeology (which revolves around the identity of the Lapita culture dating to around 3500 years ago in Melanesia), anthropologists have suggested that there were extensive contacts among Melanesian populations, interactions with other populations further west, and ultimately the development of the maritime culture that could spread into Polynesia within the past 3000 years. Depending on the magnitude of genetic contributions and cultural contributions of different populations, these models are sometimes called "tangled bank", "slow boat", "slow train", or who knows what else.

So far all of it has been a little bit arbitrary. As I noted in my class today, there is every reason to expect that these ancient populations interacted with each other extensively even there was a relatively rapid dispersal from Southeast Asia leading to the ultimate colonization of Polynesia. This means that genetic evidence may not definitively show the mode of movement -- indeed, it might be fair to say that there was no single mode, since there almost certainly would have been a reticulate pattern of migrations no matter what the linguistic or cultural origins of the movement. The key here is that cultural origins are not genetic origins, and vice versa. As anthropologists, we want to know what circumstances led people to begin the migration across the Pacific Ocean. The genetic relationships of those people address that question only very indirectly.

The new study stands apart from earlier work, in that it shows that there actually are lineages in present-day Taiwanese populations that are shared with Polynesian peoples. It is one trace that the extent of population contacts was great enough to encompass Taiwan as at least one of the origins of Polynesian populations. This evidence is not sufficient to show that the express train model happened, but it does lend reality to the idea that the cultures responsible for the beginnings of oceanic migrations may have owed much to developments on the Asian mainland.

To me, the most interesting aspect of the study is that it demonstrates a difference between the mtDNA and the Y chromosome genealogy in the region. It is somewhat difficult to imagine how mitochondrial evidence of a Taiwanese origin would survive, while Y chromosome evidence would be erased. Trejaut et al. (2005) suggest that the proto-Austronesian communities "were matriarchal and matrilocal (as the Amis tribe still is in Taiwan) whereby the Y chromosome pool of the initial migrants was lost after being repeatedly diluted on the way toward Polynesia." Maybe so. On the other hand, it would seem like a more likely scenario for the movement of a coastal, seagoing population would involve men more prominently, as young men with limited prospects and resources made risky ventures in search of greater opportunities. This would be sort of a Viking model of male behavior, although not necessarily implying conquest but merely the pursuit of new resources and mating opportunities.

If maternal lines actually remained as a stronger indicator of population origins for Polynesians, then I think we have to conclude that the population history was relatively unique. It would have to have involved the steady population growth and progressive fissioning of matriarchal communities, with little female genetic input from other groups. The maintenance of this female-centric population expansion, even as these communities spread into regions far from their initial source, would be an exceptional instance of the mediation of mating contacts by culture. The interesting part is that males presumably had extensive contact with adjacent populations, and the expanding matriarchal population apparently extensively integrated local males as it moved. In other words, the Austronesian expansion in this scenario was driven predominantly by a maternal core, even as it was surrounded by extensive expansion of other, non-maternal lineages. The main stream of maternal inputs remained central, while any initial male contributions from China or Taiwan became increasingly ephemeral.

On the other hand, there is a simpler answer available. If both these loci were affected by selection, then any difference between them would be explained in adaptive terms. There may be no reason to expect changes to these two molecules within the last 10,000 years, but if anything has been under selection certainly the mitochondrial DNA and the Y chromosome are the leading candidates. Recall that Genghis Khan's Y chromosome is supposedly in a third of Asians today -- it didn't get there by chance but by differential reproduction. There may not have been the possibility of such widespread reproduction of a single variant in the population history of Southeast Asia.

But it isn't really necessary to account for these observations. What we're seeing is a progressive increase in the frequency of a few Y chromosome alleles as we sample nearer to Polynesia. Geneticists usually look at this distribution backwards, taking the high frequency variants in Polynesia and looking for the source population in Southeast Asia or Indonesia. But this assumes that genetic drift, through successive founder effects, has been responsible for the increase in frequency of these initially rare variants.

Consider instead the scenario from the beginning to the end. How does an initially rare variant become very common in the descendants of the migrating group? Founder effects are one answer, but not the only one. What if natural selection has had a thumb on the scale from the beginning? Or what if subsequent population movement from Southeast Asia into Indonesia and Melanesia has carried advantageous Y chromosomes that have partially erased the initial distributions. Or what if an advantageous mitochondrial variant became more and more common as a result of selection in migrating populations?

The genes are far from answering these questions. Not only do we have to assume that there was no selection, but we can't even tell the various really complicated scenarios of population history apart. What's the difference between a slow boat and a slow train? How is the origin of populations of the Indian Ocean fit into this? There's a lot of work to come.

And it's for no small reason. As I lectured to my class today, the origins of oceanic populations ought to be one of the simplest problems of anthropological genetics. We're dealing with populations that are modeled well by an island model, which is unheard of in most human groups. Even so, humans have done everything possible in the past to make it difficult for us to recover that history. They mix with each other, they trade with each other, they move back and forth, they adopt new languages, and every piece of their history erases some of what has come before. So for me, the origins of Polynesians are a touchstone: if we can ever satisfactorily recover an answer, we can start to have some confidence about our ability to answer other questions that are more difficult.

References:

Trejaut JA et al. 2005. Traces of archaic mitochondrial lineages persist in Austronesian-speaking Formosan populations. PLoS Biol 3:e247. Free full text