Australia

David Reich and colleagues today report on the persistence of Denisova-like ancestry in island Southeast Asia and Australia (citation not yet available). Meanwhile, Morten Rasmussen and colleagues (citation not yet available) report on the whole-genome sequencing of hair from an Aboriginal Australian who lived some 100 years ago.

The most obvious story: These data utterly destroy the hypothesis of a single out-of-Africa colonization of Southeast Asia by modern humans. Many human geneticists have argued our present pattern of diversity originated in a wave of successive founder effects coming from a single recent African origin. They were wrong.

Instead, we can turn to a complex model with successive dispersals and episodes of population mixture. This is not a static model of isolation-by-distance; it is a dynamic model in which populations grow and spread across large spans of the Old World, again and again and again. By my count, at least three massive episodes of population dispersal and mixture are necessary in Reich and colleagues' model. A picture of their admixture hypothesis:

This model depicts (a) an early divergence of an African (represented by Yoruba) and Asian/Australasian populations. These mix with first Neandertals and then (for the Australian/New Guinea/Mamanwa populations) with Denisova-like people. Later (b), after the initial habitation of the Philippines by the ancestors of Mamanwa, a population like Andamanese Onge pushes into the islands, mixing with the ancestors of New Guinea and Australian populations. Later still (c), a population ancestral to today's Chinese people mixes with Philippines and other Southeast Asian people.

As complicated as it looks, even this model must be a vast oversimplification. I don't like or attribute much belief to mixture models like this, as they assume too much about relative population sizes and the timing of mixture. Many recent hunting and gathering populations of Southeast Asia are not included in the current samples, and the Chinese sample is itself the result of very recent demographic events, covering what once may have been a wider diversity of peoples. Depicting Australian and New Guinean populations as monolithic is an artifact of the small sample; these places themselves housed a tremendous diversity of peoples. Nevertheless, the true model won't be simpler than this one; it will involve many more events that the data cannot yet resolve.

Hints of that complexity emerge from the Aboriginal Australian whole genome. Rasmussen and colleagues show that this individual shares some ancestry with East Asian peoples, but on the whole populations in Europe and East Asia are much more genetically similar to each other than to this genome. The picture from the whole genome is essentially the same as that drawn by the SNP comparisons by Reich and colleagues, but with the potential (in the long run) to actually trace the histories of individual genes. And I think the gene-by-gene account of history will be important, because we already have some evidence that a few Denisovan genes do persist in mainland Asia, even though most are gone.

To explain why, we can look at the proportion of Denisovan ancestry in different populations as depicted in a map by Reich and colleagues. The pie charts are confusing here, because they report the fraction of ancestry from Denisovans in each population relative to the 5% estimate for New Guinea. So Australians also have 5% in this figure, Timorese have around 2.5%, and Bougainville has more than 4%.

Notice the apparent lack of Denisovan ancestry in anyone who lives anywhere that was once connected by land with mainland Asia. I say "apparent" deliberately: Abi-Rached and colleagues reported last month on the widespread distribution of Denisovan HLA types among today's Asian populations, and those may well be products of Denisovan genes that were later selected. I've already identified a handful of other loci that seem to reflect Denisovan ancestry in mainland Asian people. According to the comparisons by Reich and colleagues, such loci must be exceptions.

At the same time, the mixture model presents an important idea: Once there were people in Southeast Asia who had much more Denisovan ancestry than any populations still remaining today. Both Australian/New Guinea populations and Philippine populations like the Mamanwa have subsequently mixed with new immigrants who lacked any sign of Denisovan ancestry. Prior to this later mixture, the ancestors of those populations must have been more Denisovan -- Reich and colleagues estimate 7%. This is the first evidence that ancestry from archaic people of Eurasia was diluted to a lower value by later population movements. If the population mixture originally happened somewhere in mainland Asia, any traces of Denisovan ancestry in those areas has been diluted almost to nonexistence. But the persistence of some genes would be predicted if natural selection were maintaining them in the face of demographic pressure from elsewhere.

About the Australian genome, there will be much more interesting analyses to come, I expect. As whole-genome data come to represent more of the variation within human populations, we get a larger store of information about how we came to be variable. Variation traces not only to population movements and demography, but also to natural selection. Australia's population history has been very different from many populations of the Old World, and this genome should give us new perspective on the effects of that demographic history.

Glenn Summerhayes and colleagues [1] enter a brief report in Science this week, describing radiocarbon dates for several small archaeological assemblages from the Ivane Valley, in eastern Highland New Guinea. The abstract:

Data from the New Guinea Highlands (at an elevation of ~2000 meters) demonstrate the exploitation of the endemic nut Pandanus and yams in archaeological sites dated to 49,000 to 36,000 years ago, which are among the oldest human sites in this region. The sites also contain stone tools thought to be used to remove trees, which suggests that the early inhabitants cleared forest patches to promote the growth of useful plants.

The details of the assemblages are illuminating:

1. There are "waisted axes", large cutting tools with grooves on the sides for hafting onto wooden handles. They suggest, on ethnographic analogy, that these were used for forest clearing. I would imagine them useful for broader woodworking tasks, though, possibly including food extraction. The waisted axe artifacts here are not as extensively shaped as the later examples reported by Groube and colleagues [2]. The authors do not report on use wear for these.

2. Starch grains adhering to some of the stone tools indicate yam utilization, but yams live quite a bit lower than the site where these tools were found.

3. Lots of Pandanus nut roasting.

The dates don't make a huge impact on our understanding of the chronology. Almost 25 years ago, Groube and colleagues [2] reported TL dates with a minimum of 38,000 years ago -- and a maximum around 56,000 -- for material remains on the nearby Huon Peninsula. The current study is consistent with the range of dates reported for that site, but pushes the minimum date earlier, to around 43,000 years ago (calibrated).

The "Highland" aspect is more interesting, suggesting a fairly quick adaptability of early humans to a novel ecology. People had found the local plant foods in a unique ecology, they were exploiting a range of altitudes in their foraging activities, and possibly were altering their landscapes by forest clearing.

Or possibly, all this suggests that humans had already been in the area for a substantial length of time...

Or -- let me be even more subversive -- why is a New Guinea assemblage automatically assumed to be made by modern humans, when assemblages of equal (or greater!) technological sophistication on nearby Flores aren't?

Just asking....

References

In the current issue of Heredity, Neaves and colleagues describe the results of their analysis of 12 microsatellite loci and the mtDNA of two kangaroo species -- western and eastern grey kangaroos. The two species are sympatric across part of Australia, basically a swath through western New South Wales. Neaves and colleagues describe substantial evidence for introgression of both autosomal loci and mtDNA into both populations:

A total of 7.6% of grey kangaroos sampled from the region of sympatry displayed evidence of introgression. Although no F1 hybrids were identified, 14 M. giganteus backcrosses and 3 M. fuliginosus backcrosses were detected. In addition to introgression at nuclear microsatellite loci, a single individual also exhibited introgression of mtDNA. The two phenotypic groups apparent within the region of sympatry corresponded (in 95% of individuals) to the two clusters identified by genetic analyses. Furthermore, the two phenotypic/genetic groups within the region of sympatry corresponded to representative allopatric samples of M. giganteus and M. fuliginosus from elsewhere in the distribution. Five of the M. giganteus backcrosses identified by genetic analyses were classified as M. fuliginosus based on overall phenotype. Geographically, hybrids were located throughout the region of sympatry.

This introgression has happened between the kangaroos despite the presence of prezygotic barriers that interrupt mating even in captivity:

Physical differences in the structure of the cloacal eminence as well as the production of species-specific odours by females may allow for species recognition (Kirsch and Poole, 1972). These characteristic differences are potentially among the features that result in the unidirectional hybridization observed in captivity, with male M. giganteus frequently failing to recognize female M. fuliginosus in oestrus.

In addition, there was male sterility in captive F1 hybrids. The authors expected a unidirectional bias in introgression owing to these factors, but the evidence says that gene flow apparently has gone both directions in the wild.

Sort of interesting -- I would actually have expected there to be fewer postzygotic isolating mechanisms in marsupials because the placenta-uterus interaction isn't there complicating matters. But cases of interspecific hybridization have apparently been rarely noted -- maybe that's because Australia is small enough that phylogeographic differentiation doesn't go as far for large species. In any event, this case is another one where F1 hybrids are basically absent in the area of sympatry, yet substantial historical introgression has clearly happened. That's based on a restricted sample of 12 autosomal loci -- we would expect to see much more significant effects at a few genes if the introgressive variant had a high adaptive value.

A model for ancient humans? Well, here's a case where 12 microsatellite loci seem sufficient to document substantial historical gene flow -- whereas in the human case described last week, there are more than 600 microsatellite loci to test the hypothesis. So the human case should have more power, all things being equal.

But the humans probably don't have as simple a prior population structure. The kangaroos have two well-defined lineages with a large zone of sympatry. Ancient humans may not have been highly differentiated (given the low Neandertal-human mtDNA coalescence time, for example) and may not have had substantial zones of sympatry -- they may have been much more similar populations interacting along a narrow boundary or cline. So the phylogeography in humans will be much more subtle.

References:

Neaves LE, Zenger KR, Cooper DW, Eldridge MDB. 2010. Molecular detection of hybridization between sympatric kangaroo species in south-eastern Australia. Heredity 104:502-512. doi:10.1038/hdy.2009.137