September 30, 2011

"Comparing Ancient and Modern DNA Variability in Human Populations" abstracts

Excerpts from the conference site.

Temporal differentiation across a West-European Y-chromosomal cline - genealogy as a tool in human population genetics
Maarten H.D. Larmuseau et al.
The pattern of population genetic variation and allele frequencies within a species are unstable and are changing in time according to different evolutionary factors. For humans, it is possible to combine detailed patrilineal genealogical records with deep Y-chromosome genotyping to disentangle signals of historical population genetic structures due to the exponential increase of genetic genealogical data. To test this approach we studied the temporal pattern of the 'autochthonous' micro-geographical genetic structure in the region of Brabant in Belgium and The Netherlands (Northwest-Europe). Genealogical data of 881 individuals from Northwest-Europe were collected from which 634 family trees showed a residence within Brabant for at least one generation. The Y-chromosome genetic variation of the 634 participants was investigated using 110 Y-SNPs and 38 Y-STRs and linked to particular locations within Brabant on specific time periods based on genealogical records. Significant temporal variation in the Y-chromosome distribution was detected through a north-south gradient in the frequencies distribution of subhaplogroup R1b1b2a1 (R-U106), next to an opposite trend for R1b1b2a2g (R-152). The gradient on R-U106 faded in time and became even totally invisible during the Industrial revolution in the first half of the 19th century. Therefore, genealogical data for at least 200 year are required to study small-scale 'autochthonous' population structure in Western-Europe.
The Dutch medieval and post-medieval genetic landscapes
Eveline Altena et al.
Since 2005 many archeological human skeletons have been sampled for DNA research under forensic conditions in The Netherlands. This enables us to perform a large scale genetic survey on reliable genetic data from the prehistory until the present. The majority of the available archaeological DNA samples, though, originate from medieval and post-medieval sites. Here we present preliminary autosomal and Y-chromosomal data from more then 500 archaeological human skeletons, excavated at several medieval and post-medieval sites. We also compare these historical genetic data with data from more then 2000 modern Dutch males.
Comparing ancient and modern DNA variability in North Eastern Iberia: the Neolithic impact of first farmers
Cristina Gamba et al.
Archaeological, anthropological and demographic hypotheses can be tested by comparing ancient and modern DNA from human samples in a diachronical context. In this case, it was possible to evaluate genetic continuity or discontinuity between different periods, and/or to infer ancient human migrations in a set of Iberian samples. We evaluated the demographic impact associated to the spread of the Neolithic in North Eastern Iberia. We recovered mitochondrial DNA from 13 Early Neolithic specimens from three archaeological sites: Can Sadurní, Chaves and Sant Pau. A bayesian simulation approach was performed to compare the obtained results with Middle Neolithic and modern samples from the same region. We tested different scenarios to determine which among them better explained the analyzed data. By comparing simulated and observed FST values, we observed genetic differentiation between Early Neolithic and Middle Neolithic populations, which suggests that at the beginning of the Neolithic, genetic drift played an important role.
Genetic differentiation was also observed between Early Neolithic and modern- day populations. These data are compatible with the arrival of small genetically-distinctive groups at the beginning of the Neolithic, suggesting a pioneer colonization of North Eastern Iberia by first farmers.
The following abstract is interesting as it suggests we should not view the "Neolithic" as a singular event. X2 was also discovered in Megalithic France, as well as a likely immigrant population from the Near East and the Caucasus in the Tarim Basin, and Bronze Age Eulau. From a paper on the Reidla et al. (2003): Overall, it appears that the populations of the Near East, the Caucasus, and Mediterranean Europe harbor subhaplogroup X2 at higher frequencies than those of northern and northeastern Europe (P less than .05) and that X2 is rare in Eastern European as well as Central Asian, Siberian, and Indian populations and is virtually absent in the Finno-Ugric and Turkic-speaking people of the Volga-Ural region.

Where are all the "WIX"? Rare European maternal lineages W, I, and X2 in the past and present
Esther J. Lee et al.
Studies utilizing ancient DNA to examine past populations in Europe have increased dramatically in recent years. Specifically, mitochondrial DNA (mtDNA) sequences for over 100 individuals in prehistoric Europe have been sequenced and published. Scholars have intensively focused on the so-called Neolithic transition in Europe, the transformation from hunter-gatherer lifestyle to agro-pastoralism, and continue to debate whether the process was a result of population movement or cultural dispersion. Both hypotheses continue to be tested and genetics analyses from past and present populations have suggested a complex movement of people and cultures across Eurasia. This work focuses on the mtDNA haplogroups identified in past European populations that are rare in the present, haplogroups W, I, and X2. New data will be presented from Neolithic Funnel Beaker collective burials sites, a late Neolithic Bell Beaker site, and an Iron Age Halstatt site in Germany, in which the three maternal lineages are identified. Among the published European Neolithic data, haplogroup X2 appears in late Neolithic sites in Germany and France but not in the earlier LBK culture. Haplogroup X2 shows an intriguing phylogenetic landscape with a wide geographical distribution at an overall low frequency, but on the other hand, pockets of high diversity and frequency among certain modern western Eurasian populations have been described. The discussion focuses on whether the presence of the three haplogroups in the past is a result of ascertainment bias or some viable population movement.
The following seems to suggest Denisova admixture in the East Asian mainland, and not just the island groups, identified in the recent Reich et al. (2011) paper. The sentence about biased Neandertal similarity with increasing distance to Africa is also interesting; the data that is available so far shows non significant differences in Neandertal similarity among Eurasians, although the published values do seem to show higher (and perplexing) averages in China vs. Europe.

Archaic human ancestry in East Asia
Pontus Skoglund & Mattias Jakobsson
Recent studies of ancient genomes have suggested that gene flow from archaic hominin groups to the ancestors of modern humans occurred on two separate occasions during the modern human expansion out of Africa. At the same time, decreasing levels of human genetic diversity have been found at increasing distance from Africa as a consequence of human expansion out of Africa. We re-analyzed the signal of archaic ancestry in modern human populations and we investigated how serial founder models of human expansion affect the signal of archaic ancestry using simulations. We show that genetic drift coupled with an ascertainment bias for common alleles can cause artificial, but largely predictable, differences in affinity to archaic genomes between descendants of an admixture event. In genotype data from non-African humans, this effect results in a biased genetic similarity to Neandertal with increasing distance from Africa. In addition to the two previously reported connections between non-Africans and Neandertals as well as between Oceanians and a Denisovan archaic human genome from Siberia, we found a significant affinity between East Asians (in particular Southeast Asians) and the Denisovan genome, a pattern that is not expected under a model of solely Neandertal-related admixture in the ancestry of East Asians. This observation could be explained either by substantial migration from Oceania into East Asia, or more common history between anatomically modern- and archaic populations than previously proposed.

September 29, 2011

Diet of Byzantine Greeks

AJPA DOI: 10.1002/ajpa.21601

Reconstructing the diets of Greek Byzantine populations (6th–15th centuries AD) using carbon and nitrogen stable isotope ratios

Chryssi Bourbou et al.

Documentary evidence and artistic representations have traditionally served as the primary sources of information about Byzantine diet. According to these sources, Byzantine diet was based on grain (primarily wheat and barley), oil, and wine, supplemented with legumes, dairy products, meat, and marine resources. Here, we synthesize and compare the results of stable isotope ratio analyses of eight Greek Byzantine populations (6th–15th centuries AD) from throughout Greece. The δ13C and δ15N values are tightly clustered, suggesting that all of these populations likely consumed a broadly similar diet. Both inland and coastal Byzantine populations consumed an essentially land-based C3 diet, significant amounts of animal protein, and possibly some C4 plants, while no evidence of a general dependence on low-δ15N legumes was observed. One interesting result observed in the isotopic data is the evidence for the consumption of marine protein at both coastal sites (a reasonable expectation given their location) and for some individuals from inland sites. This pattern contrasts with previous isotopic studies mainly on prehistoric Greek populations, which have suggested that marine species contributed little, or not at all, to the diet. The possibility that fasting practices contributed to marine protein consumption in the period is discussed, as are possible parallels with published isotope data from western European medieval sites.


No higher borrowing in hunter gatherer languages

PLoS ONE 6(9): e25195. doi:10.1371/journal.pone.0025195

Does Lateral Transmission Obscure Inheritance in Hunter-Gatherer Languages?

Claire Bowern et al.

In recent years, linguists have begun to increasingly rely on quantitative phylogenetic approaches to examine language evolution. Some linguists have questioned the suitability of phylogenetic approaches on the grounds that linguistic evolution is largely reticulate due to extensive lateral transmission, or borrowing, among languages. The problem may be particularly pronounced in hunter-gatherer languages, where the conventional wisdom among many linguists is that lexical borrowing rates are so high that tree building approaches cannot provide meaningful insights into evolutionary processes. However, this claim has never been systematically evaluated, in large part because suitable data were unavailable. In addition, little is known about the subsistence, demographic, ecological, and social factors that might mediate variation in rates of borrowing among languages. Here, we evaluate these claims with a large sample of hunter-gatherer languages from three regions around the world. In this study, a list of 204 basic vocabulary items was collected for 122 hunter-gatherer and small-scale cultivator languages from three ecologically diverse case study areas: northern Australia, northwest Amazonia, and California and the Great Basin. Words were rigorously coded for etymological (inheritance) status, and loan rates were calculated. Loan rate variability was examined with respect to language area, subsistence mode, and population size, density, and mobility; these results were then compared to the sample of 41 primarily agriculturalist languages in [1]. Though loan levels varied both within and among regions, they were generally low in all regions (mean 5.06%, median 2.49%, and SD 7.56), despite substantial demographic, ecological, and social variation. Amazonian levels were uniformly very low, with no language exhibiting more than 4%. Rates were low but more variable in the other two study regions, in part because of several outlier languages where rates of borrowing were especially high. High mobility, prestige asymmetries, and language shift may contribute to the high rates in these outliers. No support was found for claims that hunter-gatherer languages borrow more than agriculturalist languages. These results debunk the myth of high borrowing in hunter-gatherer languages and suggest that the evolution of these languages is governed by the same type of rules as those operating in large-scale agriculturalist speech communities. The results also show that local factors are likely to be more critical than general processes in determining high (or low) loan rates.


September 28, 2011

Aboriginal genome analysis and ethics

Ewen Callaway discusses ethical issues surrounding the publication of an Australian Aborigine full genome sequence from a hair sample collected about a hundred years ago by a British scientist.

From the article:
"To be sequencing DNA from the hair of a deceased indigenous person is uncharted ethical territory," says Emma Kowal, a cultural anthropologist at the University of Melbourne.
Sequencing DNA from the hair of a deceased indigenous person is nothing new. Scientists have done it, for example, on Napoleon's hair. But, of course, "indigenous", is a code word for pre-European. Everyone's genome is a composite of bits that have arrived at different times from different places. There is nothing "indigenous" about any of our DNA, unless we believe in fables like that of Erichthonius. What is the use of the concept of "indigeneity"? To make cultural anthropologists feel good about their role as protectors of "indigenous people".

Of course, I believe that anthropologists should not just go ahead and get DNA from the dead. But, as far as I can tell, Haddon did not go around the world with a pair of scissors chasing after people for hair samples. Nor are there, as far as I can tell, any close relatives of the deceased that might object to his full genomic sequence (and by implication half, or a quarter of their sequence) being published. So, where is the ethical problem?

More from the article:
But some scientists are jittery about how others in the Aboriginal community might receive the project, and worry that it could set back efforts to engage Aboriginals in genetic research. "In a sense, every Aboriginal Australian has had something about themselves revealed to the world without their consent," says Hank Greely, who directs the Center for Law and the Biosciences at Stanford University in California.
In other words: let's not do genetic research because it might prevent us from doing genetic research. Of course something has been revealed about Aboriginal Australians by the use of this sample. Something has been revealed about me whenever there are Greek DNA samples published. There have been tons of genetic studies on Jews, Finns, African Americans, etc., should we seek the "consent" of every group one belongs to before doing a study? I'm human, and I object to studies comparing humans with chimpanzees, because it might reveal something about me without my consent...

Aboriginal Australians endured centuries of repression by European colonists, but their wariness of genetic research owes much to the Human Genome Diversity Project (HGDP). This 1990s international collaboration aimed to catalogue the genetic diversity of populations worldwide, but sparked concerns that indigenous peoples were being subjected to neocolonial 'bioprospecting'. "Probably the strongest opposition we ran into anywhere in the world" was in Australia, says Greely, who was an ethical adviser to the project. Plans to include Aboriginal Australian DNA were eventually scrapped, and the furore's impact continues to reverberate, says Kowal. "The damage that the HGDP has done for the prospect of doing genetic research with Aboriginal people has been significant." Researchers who work with Aboriginal Australians are now expected to obtain consent not only from the individuals concerned, but also from local and sometimes state-wide groups representing Aboriginal communities across Australia.
I believe in empirical evidence. There are dozens of human populations represented in the Human Genome Diversity Panel that have been used and re-used by scientists and amateurs like myself alike. Can any of the professional kind souls point to a single bad thing that has happened to any of these populations because of it?

What about the rights of individual Aboriginal Australians? Suppose that you are an Aboriginal Australian who wants to learn about his ancestry and origins, the same with all those Europeans, Africans, Asians, etc. who buy genetic ancestry tests or visit genealogy, archaeology, and history forums. Why should your natural desire to learn about your own past, and the natural desire of anthropologists and geneticists to learn about human history have to go through the bureaucracy of community- and state-level "representatives"?

A Danish bioethical review board did not believe it was necessary to review the project because it viewed the hair as an archaeological specimen and not a biological one, Willerslev says. However, after his team sequenced the genome, an Australian colleague put Willerslev in touch with the Goldfields Land and Sea Council, a body based in Kalgoorlie, Western Australia, that represents the 5,000 or so Aboriginal Australians living in the region where Haddon collected the hair sample. In June, Willerslev flew to the region to describe his project to the organization's board and to seek its approval. He says that if the board had rejected his proposal, he would have ended the project and left the genome unpublished.
I am glad that the "Land and Sea Council" gave Willerslev its consent. But, seriously, who are they to decide whether the hair sample should be used or not?

It could be argued that Haddon's unknown hair donor did not authorize a particular use of his hair sample. But, it is ludicrous to expect people from the past to anticipate all the potential uses that their tissues may have in the future. Nor is there any evidence that the anonymous donor authorized some council representing 5,000 future Aboriginal Australians, including a few of his distant relatives to prevent it from being used.

Despite Willerslev's efforts, "I would suggest there would be a certain amount of unrest in the indigenous communities", says van Holst Pellekaan. Greely agrees that Willerslev's team should have reached out to other Aboriginal groups.
So, it is not only sufficient for the future local council to get in on the consent action, but it is proposed that the one from the next town, or halfway around Australia should be involved too.

Scientists should not victimize DNA donors or their communities, but neither should they acquiesce to a never-ending political game of "consent", whereby they must appease every busybody elected or unelected "representative" before doing their work.

Mark Stoneking has it about right:
"I think they did everything anyone could reasonably expect them to," counters Mark Stoneking, a molecular anthropologist at the Max Planck Institute for Evolutionary Anthropology in Leipzig, Germany. He published a complementary analysis of Aboriginal genomes last week, using DNA samples obtained by other scientists with the consent of the Aboriginal Australian individuals involved.
But, I would argue that they did more than anyone could reasonably expect them to. Since there is no evidence that the sample was collected illegally and unethically, and since the Danish review board approved the study, there would have been no reason not to publish the study if the "Goldfields Land and Sea Council" had objected. I would be pissed if I was a member of the research group that did all this work without intending or actually causing harm to anybody, and I was told not to publish because some council said so.

Moreover, the issue is one of basic scientific integrity: scientists should seek to understand the world as it is, including patterns of human diversity and history.

Suppose that Willerslev had reached a different conclusion, e.g., that Australian Aborigines arrived 5,000 years ago, and this was rejected by local interest groups because it clashed with their oral histories. Are scientists only to publish results that are acceptable to studied populations' traditions and mythologies, and be prevented from publishing those that falsify them?

Having a set of widely accepted guidelines for studying such samples would help to guide researchers, journals and funding agencies, says Stoneking. "Hopefully some sort of standards can be developed so everyone feels comfortable going ahead with this research," he says.
I agree. A set of guidelines would have twofold utility:
  1. To prevent researchers from engaging in unethical behavior. We don't want scientists to get people's DNA and then use it against them in a demeaning manner, or profiting from its potential commercial uses.
  2. To prevent professional complainers from stopping scientific research when it might or does clash with local lore or ill-defined interests

September 27, 2011

Uzbeks as the nexus, Altai as the source of Turkic expansions

I have often used Uzbeks as a convenient population to assess the extent of Central Asian Turkic admixture in West Eurasia. The recent Yunusbayev et al. (2011) paper has provided some interesting supporting evidence for that use:

I have extended lines from Uzbeks through the four different western Eurasians Turkic populations: Turks, Turkmen, Nogais, and Chuvashs. It is interesting that these lines intersect West Eurasians at different points:
  • The line of Turks (Anatolia) with Armenians and Georgians
  • The line of Turkmen (Iran) with Iranians
  • The line of Nogais (North Caucasus) with Chechens
  • The line of Chuvashs (far eastern Europe) beyond Russians
These are what we expect if ancestral Turkic speakers en route from their ultimate eastern homeland were roughly like modern-day Uzbeks at some stage before their settlement in west Eurasia. The linearity of the Uzbek-Turkic population-Native population triples is striking

The only case where the fit is not almost perfect is that of the Chuvashs, who are the most northern population. It is easy enough to discover the cause of this. Chuvash have ~1.1% South Asian, as opposed to ~8.2% in the Uzbeks. There is a north-south latitudinal cline of the "South Asian" component in middle Eurasia, and the ancestors of the Chuvash moved at the northern end of that cline; of the Uzbeks at the middle.

If we add a line linking Russians with Chuvashs, we can reconstruct the hypothetical Proto-Chuvashs as a population that differed from Uzbeks in being less "South Asian", which confirms the Dodecad admixture data:

The mystery is further resolved once we look at the following PCA plot from my article On the northern/southern Caucasoid contributions to Asia

Notice that Turks, Uzbeks and the pair of Altai and Dolgan fall along one line, while Chuvashs, Russians, and the pair of Altai/Dolgan along another.

So, the data seems consistent with the idea that the primary source of the westward Turkic expansions was something like the Altai (pics) and Dolgan, undergoing transformations and successive admixtures all the way to the Mediterranean and eastern Europe.

September 26, 2011

mtDNA of Oceanians (Ballantyne et al. 2011)

Forensic Sci Int Genet. 2011 Sep 20. [Epub ahead of print]

MtDNA SNP multiplexes for efficient inference of matrilineal genetic ancestry within Oceania.

Ballantyne KN, van Oven M, Ralf A, Stoneking M, Mitchell RJ, van Oorschot RA, Kayser M.


Human mitochondrial DNA (mtDNA) is a convenient marker for tracing matrilineal bio-geographic ancestry and is widely applied in forensic, genealogical and anthropological studies. In forensic applications, DNA-based ancestry inference can be useful for finding unknown suspects by concentrating police investigations in cases where autosomal STR profiling was unable to provide a match, or can help provide clues in missing person identification. Although multiplexed mtDNA single nucleotide polymorphism (SNP) assays to infer matrilineal ancestry at a (near) continental level are already available, such tools are lacking for the Oceania region. Here, we have developed a hierarchical system of three SNaPshot multiplexes for genotyping 26 SNPs defining all major mtDNA haplogroups for Oceania (including Australia, Near Oceania and Remote Oceania). With this system, it was possible to conclusively assign 74% of Oceanian individuals to their Oceanian matrilineal ancestry in an established literature database (after correcting for obvious external admixture). Furthermore, in a set of 161 genotyped individuals collected in Australia, Papua New Guinea and Fiji, 87.6% were conclusively assigned an Oceanian matrilineal origin. For the remaining 12.4% of the genotyped samples either a Eurasian origin was detected indicating likely European admixture (1.9%), the identified haplogroups are shared between Oceania and S/SE-Asia (5%), or the SNPs applied did not allow a geographic inference to be assigned (5.6%). Sub-regional assignment within Oceania was possible for 32.9% of the individuals genotyped: 49.5% of Australians were assigned an Australian origin and 13.7% of the Papua New Guineans were assigned a Near Oceanian origin, although none of the Fijians could be assigned a specific Remote Oceanian origin. The low assignment rates of Near and Remote Oceania are explained by recent migrations from Asia via Near Oceania into Remote Oceania. Combining the mtDNA multiplexes for Oceania introduced here with those we developed earlier for all other continental regions, global matrilineal bio-geographic ancestry assignment from DNA is now achievable in a highly efficient way that is also suitable for applications with limited material such as forensic case work.


September 23, 2011

Bronze age Y-chromosomes and mtDNA from Liao River (northern China)

From the paper:
The dominant haplogroup in the Dadianzi people was D4 shared by
five individuals who were associated with four different haplotypes.

The other haplotype belonging to haplogroup D in the Dadianzi population
was designated as D5 by the mutation at site 16 189 (T to C).
The haplogroup M7c included two haplotypes, which were shared by two
individuals in ancient Dadianzi people. The other haplogroups, including
A4, F1b, G1a, M9a, M10 and M8z, were each present in one individual.

Seven male samples were chosen for Y chromosome SNPs among
the 14 individuals. Three samples (S1, S2 and S13) exhibited the
mutations M89C-T, M9C-G, M214T-C and M231G-A, which
were attributed to haplogroup N ( N1C). Two samples (S8 and S12)
exhibited the mutations: M89C-T, M9C-G, M175-5 bp del and
M122T-C, belonging to haplogroup O3 (M122). We failed to obtain
any product from two samples (S5 and S14) (Table 3).

Journal of Human Genetics advance online publication 22 September 2011; doi: 10.1038/jhg.2011.102

Genetic characteristics and migration history of a bronze culture population in the West Liao-River valley revealed by ancient DNA

Hongjie Li et al.

In order to study the genetic characteristics of the Lower Xiajiadian culture (LXC) population, a main bronze culture branch in northern China dated 4500–3500 years ago, two uniparentally inherited markers, mitochondrial DNA and Y-chromosome single-nucleotide polymorphisms (Y-SNPs), were analyzed on 14 human remains excavated from the Dadianzi site. The 14 sequences, which contained 13 haplotypes, were assigned to 9 haplogroups, and Y-SNP typing of 5 male individuals assigned them to haplogroups N (M231) and O3 (M122). The results indicate that the LXC population mainly included people carrying haplogroups from northern Asia who had lived in this region since the Neolithic period, as well as genetic evidence of immigration from the Central Plain. Later in the Bronze Age, part of the population migrated to the south away from a cooler climate, which ultimately influenced the gene pool in the Central Plain. Thus, climate change is an important factor, which drove the population migration during the Bronze Age in northern China. Based on these results, the local genetic continuity did not seem to be affected by outward migration, although more data are needed especially from other ancient populations to determine the influence of return migration on genetic continuity.

September 22, 2011

Unexpected ancient mtDNA from Neolithic Hungary

This seems like a tie-in to another recent post on Neolithic and Bronze Age Ukraine. I don't think even a science fiction writer could have predicted the kinds of ancient DNA results we are getting from Europe. We have genetic discontinuity between Paleolithic and Neolithic, and between Neolithic and present, and, apparently, discontinuity between Neolithic cultures themselves, and wholly unexpected links to East Asia all the way to Central Europe.

When faced with data such as this, one can only say: what the hell happened during European prehistory?

UPDATE (8 Jun 2012): The age of these remains has been questioned.

Journal of Human Genetics advance online publication 15 September 2011; doi: 10.1038/jhg.2011.103

HVS-I polymorphism screening of ancient human mitochondrial DNA provides evidence for N9a discontinuity and East Asian haplogroups in the Neolithic Hungary

Zsuzsanna Guba et al.

Analysis of mitochondrial mutations in the HVS-I region is an effective method for ancient human populational studies. Discontinuous haplotype data between the first farmers and contemporary Europeans has been described before. Our contribution is based on a survey initiated on the Neolithic skeletons from Hungarian archaeological sites in the Alföld. This Lowland, the Hungarian Plain, is well excavated as an important region for spread of Neolithic culture from Near East and Balkans toward Central and Western Europe, started circa 8000 years ago. HVS-I sequences from nt15977 to nt16430 of 11 such specimens with sufficient mitochondrial DNA preservation among an extended Neolithic collection were analysed for polymorphisms, identifying 23 different ones. After assigning all single-nucleotide polymorphisms, a novel, N9a, N1a, C5, D1/G1a, M/R24 haplogroups were determined. On mitochondrial control mutations at nt16257 and nt16261, polymorphic PCRs were carried out to assess their distribution in remains. Neolithic data set was compared with contemporary Vác samples and references, resulting in higher frequency of N9a in Alföld as a remarkable genetic discontinuity. Our investigation is the first to study mutations form Neolithic of Hungary, resulting in an outcome of Far Eastern haplogroups in the Carpathian Basin. It is worth further investigation as a non-descendant theory, instead of a continuous population history, supporting genetic gaps between ancient and recent human populations.


First aboriginal Australian genome published

Aboriginal Australians (AA) have been somewhat of a black hole in population genetics research. So, it's great news that after today's Reich et al. paper on Denisova admixture, there is another new paper that presents the first full genome sequence of an aboriginal Australian.

I don't know why it has been so difficult to study AAs so far; my guess is that some type of politics has prevented it, similar to those that have hindered population genetics research in some Amerindian groups. Unfortunately, the current publication does not seem to represent the beginning of a new era in AA research, as the genome does not belong to a living AA, but rather to a 100-year old hair sample.

On one hand this makes sense: old DNA is preferable to fresh one when one deals with populations that have undergone admixture in recent times. I don't know how many AA have European admixture, but my guess is that, surely, pure-blooded living AA still exist, so, one could in principle obtain DNA from them.

Nonetheless, we should be thankful for the new data which provide a much needed new data point of mankind's diversity. Also, given recent developments, even a single genome may prove to be invaluable.

The supplementary material (pdf) has, as usual, most of the interesting details of the paper.

Coverage in the Australian.

(to be continued)

UPDATE: I will take the age estimates in the paper with a grain of salt, because they are not independent estimates, but rely on a calibration of the European-East Asian split (fixed at 2,000 generations), and the Out-of-Africa event (fixed at 3,500 generations). Hence, from the supplement:
Based on how our model was set up, the European-Aboriginal Australian and African-Aboriginal Australian split times that we presented above could be no less than 2,000 and 3,500 generations ago, respectively.
So, at most the data shows that Europeans are closer related to East Asians than either of them is to Australian aboriginals. The actual ages in years are conditioned on the timing of the aforementioned events, which, in turn, have been estimated in the past using various assumptions (see my recent post on Gronau et al. 2011).

Science DOI: 10.1126/science.1211177

An Aboriginal Australian Genome Reveals Separate Human Dispersals into Asia

Morten Rasmussen et al.


We present an Aboriginal Australian genomic sequence obtained from a 100-year-old lock of hair donated by an Aboriginal man from southern Western Australia in the early 20th century. We detect no evidence of European admixture and estimate contamination levels to be below 0.5%. We show that Aboriginal Australians are descendants of an early human dispersal into eastern Asia, possibly 62,000 to 75,000 years ago. This dispersal is separate from the one that gave rise to modern Asians 25,000 to 38,000 years ago. We also find evidence of gene flow between populations of the two dispersal waves prior to the divergence of Native Americans from modern Asian ancestors. Our findings support the hypothesis that present-day Aboriginal Australians descend from the earliest humans to occupy Australia, likely representing one of the oldest continuous populations outside Africa.


Widespread Denisovan admixture (Reich et al. 2011)

Table S2 from the paper (pdf) gives the Denisova admixture as a fraction of the Papuan New Guinea highlander Denisova admixture. It seemed almost certain to me that Australian aboriginals would register such admixture, as they have often been described, on physical anthropological grounds, as closer to Papuans than to any other human population. But, it is nice to see the evidence (or lack thereof) for Denisova admixture quantified in various groups described as "Negrito" or "Australoid" by traditional physical anthropology.

The inference, by the authors, that Denisova admixture took place in Southeast Asia itself makes sense to me. This admixture may have been variable to begin with, but it was reduced in Southeast Asia itself as the number of modern humans in it grew, absorbing the Denisova-admixed early inhabitants, with the latest episode taking the form of the arrival of East Eurasian populations (traditional Mongoloids) that seem to lack this admixture altogether.

The interesting question now seems to be: with Denisovans spread from the Altai to Southeast Asia, how did the ancestors of East Asians avoid having any?

UPDATE: Figure 1 from the paper shows Denisovan admixture as a fraction of that in New Guineans:
One of the most interesting findings of the paper is that the extent of Denisova admixture is strongly correlated with the extent of Near Oceanian (Australian-Papuan) admixture.

An interesting question is to what extent does Denisova admixture contribute to the differentiation between Australasians and other modern humans? The following admixture graph gives an idea:

You can see that 7% Denisova introgression into the ancestors of Australians/New Guineans is inferred to have been "diluted" by roughly 50-50 admixture with Denisova-deficient modern humans, leading to the ~4% figure of Denisova admixture in extant Australians/New Guineans. This was further diluted in populations like Mamanwa, by admixture with East Asians.

It seems likely that inter-population differentiation within the species H. sapiens may be driven, at least in part, by admixture with archaic humans, and is not only the result of isolation post-Out of Africa. If Franz Weidenreich were alive, he would probably be smiling.

UPDATE II: A possible reason why East Asians lack Denisovan admixture is given by Mark Stoneking, as quoted in Nature:
Stoneking says that this pattern hints at at least two waves of human migration into Asia: an early trek that included the ancestors of contemporary Aboriginal Australians, New Guineans and some other Oceanians, followed by a second wave that gave rise to the present residents of mainland Asia. Some members of the first wave (though not all of them) interbred with Denisovans. However, the Denisovans may have vanished by the time the second Asian migrants arrived. This also suggests that the Denisovan's range, so far linked only to a cave in southern Siberia, once extended to Southeast Asia and perhaps Oceania.
Given that the Denisova hominin is about 41ka old, that would imply that East Asian ancestors moved through their territory after that date, when the Denisovans were already extinct, partially absorbed by first-wave "Australasian-like" people.

We must also consider the possibility that the Denisovans themselves may have been intrusive to Siberia; could the Altai Denisovans be remnants of a Southeast Asian population that fled out of the way of the modern humans that migrated to Australasia? If that is the case, then East Asian ancestors may lack Denisovan admixture because they had already reached the far east when Denisovans started moving north.

I, for one, can't wait until we start getting ancient DNA from Upper Paleolithic H. sapiens, who knows what new surprises are in store for us?

The American Journal of Human Genetics, 22 September 2011

Denisova Admixture and the First Modern Human Dispersals into Southeast Asia and Oceania

David Reich et al.

It has recently been shown that ancestors of New Guineans and Bougainville Islanders have inherited a proportion of their ancestry from Denisovans, an archaic hominin group from Siberia. However, only a sparse sampling of populations from Southeast Asia and Oceania were analyzed. Here, we quantify Denisova admixture in 33 additional populations from Asia and Oceania. Aboriginal Australians, Near Oceanians, Polynesians, Fijians, east Indonesians, and Mamanwa (a “Negrito” group from the Philippines) have all inherited genetic material from Denisovans, but mainland East Asians, western Indonesians, Jehai (a Negrito group from Malaysia), and Onge (a Negrito group from the Andaman Islands) have not. These results indicate that Denisova gene flow occurred into the common ancestors of New Guineans, Australians, and Mamanwa but not into the ancestors of the Jehai and Onge and suggest that relatives of present-day East Asians were not in Southeast Asia when the Denisova gene flow occurred. Our finding that descendants of the earliest inhabitants of Southeast Asia do not all harbor Denisova admixture is inconsistent with a history in which the Denisova interbreeding occurred in mainland Asia and then spread over Southeast Asia, leading to all its earliest modern human inhabitants. Instead, the data can be most parsimoniously explained if the Denisova gene flow occurred in Southeast Asia itself. Thus, archaic Denisovans must have lived over an extraordinarily broad geographic and ecological range, from Siberia to tropical Asia.


September 19, 2011

Inference of ancient human demography from individual genomes (Gronau et al. 2011)

This new paper is reminiscent of Li & Durbin (2011), in that it also fits a model of ancient human demography based on individual genome sequences. Unlike that paper, it also considers a San individual, and is hence a good realization of the project I proposed in response to the Li & Durbin paper.

As is so often the case, the absolute age estimates are based on a calibration, which is spelled out quite nicely in the supplementary material (pdf; p. 55). In particular, the age estimates are based on:
  • Human-chimp divergence of 6.5Mya
  • Generation length of 25 years
As the authors note, their calibration results in:
an adjusted estimate of the per generation mutation rate would be slightly more than 2 × 10−8 mutations per site. This adjusted estimate agrees well with independent estimates of 1.8–2.5 ×10−8 (Nachman and Crowell, 2000; Kondrashov, 2003). It is slightly higher than recently reported estimates of 1.0–1.3 ×10−8 (The 1000 Genomes Project Consortium, 2010; Lynch, 2010; Roach et al., 2010), but, considering the many sources of uncertainty in these studies, we do not regard this difference as a serious concern. It is difficult to reconcile per-generation mutation rate estimates as low as 1×10−8 with the observed levels of human/chimpanzee genomic divergence.
However, Nachman & Crowell do not provide a mutation rate estimate independent of demography. As can be seen from Table 3 of their paper, their mutation rate estimate depends on human-chimp speciation as well as assumptions on ancestral effective population size. First, they assume a generation length of 20 years, hence their calibrations need to be scaled: 6.5My in 25y generations is equivalent to 5.2My in 20y generations. Nachman and Crowell estimate the mutation rate at 2.5x10-8 and 1.4x10-8 with an effective size of 10,000 individuals and speciation at 5 or 5.5Mya.

Hence, their mutation rate estimate for 5.2My would be between 1.4x10-8 and 2.5x10-8, i.e., close to the value of Gronau et al. (2011), assuming that the effective population size was 10,000 individuals. Gronau et al. estimate the effective population size at 9,000 individuals. So, there is nothing independent about N&C's age estimate: it is dependent on the effective population size, and the Gronau et al.'s mutation rate/effective size estimate of 2.0x10-8/9,000 individuals may be consistent with the data, but so is a lower mutation rate and higher effective size.

Note that, unlike Li & Durbin, Gronau et al. do not consider a model with a structured African population, or the presence of archaic admixture. These would have produced observed divergence times by a combination of a younger divergence between modern human groups, coupled with admixture with a more distantly diverged (archaic or "Palaeoafrican") population, for which there is now genetic and palaeoanthropological evidence.

I do not have a strong opinion how the 2-fold mutation rate difference between different papers will be resolved. If the slower empirical estimates are accepted, then this would result in deeper divergences between human populations, as well as an earlier human-chimp split, but the difference is not necessarily linear.

As I have noted before, there is no reason I can think of why parent-offspring rates should be slower than evolutionary ones. Two potential processes might actually make them appear faster: phantom mutations based on current whole genome sequencing technology, or loss of mutations due to drift across geological time scales. So, unless there is a technical reason for the low 1000Genomes rate, I'm more inclined to trust it rather than circular calibrations of demography/mutation rate/effective population size. In any case, we will have more full genome sequences from family members in the coming years, so the mutation rate will be calibrated directly, without recourse to human-chimp speciation or ancestral population sizes.

A slower mutation rate would make sense to me on palaeoanthropological grounds:
  • The authors estimate European/East Asian divergence at 30-45kya. But, the presence of clearly derived Caucasoid morphology in the Upper Paleolithic population of Europe, suggests to me that divergence may have begun some time before.
  • Table S2 of adjusted Mahalanobis distances from Harvati et al. (2011) leaves little doubt that the Eurasian anatomically modern humans (EAM) from the Levant (Skhul/Qafzeh) are related to subsequent Eurasians. EAM has a distance of -0.25 to later Upper Cave from China (UC); 6.42 to recent Oceanians (OCE); 7.19 to Upper Paleolithic Eurasians. All of the above are well-within the maximum divergence observed between any two modern human groups. Ancestral Eurasians likely lived before 100ky, and did not split from Africans only 50ky.
  • If there was a long isolation between Khoe-San and the rest of mankind, then where did it happen? It is no longer plausible to postulate multiple fully modern groups in Africa that are absolutely absent from the palaeoanthropological record in the timeframe in question, in reproductive isolation to the multiple archaic or archaic-like ones that keep turning up.
  • How did the ur-humans in Africa manage reproductive isolation for tens of thousands of years between themselves (Khoe-San vs. rest or moderns vs. archaics), but apparently mixed a-plenty right after they left Africa with Neandertals/Denisovans? Were Neandertal women really that sexy?
  • Actually, the fragmentary record, as it stands, has not revealed any traces of a Proto-San population, and the Hofmeyr skull from South Africa stands as an outlier in the African paleoanthropological record with its strong affinities to Upper Paleolithic Eurasians.
We are only now beginning to harness the power of full human genomes for evolutionary inferences, but it is inevitable that a new theory of human origins will appear that will reconcile the different and conflicting lines of evidence. That theory must take into account latent admixture as a cause of African genetic diversity, and it must also harmonize with the paleoanthropological record.

Nature Genetics (2011) doi:10.1038/ng.937

Bayesian inference of ancient human demography from individual genome sequences

Ilan Gronau et al.

Whole-genome sequences provide a rich source of information about human evolution. Here we describe an effort to estimate key evolutionary parameters based on the whole-genome sequences of six individuals from diverse human populations. We used a Bayesian, coalescent-based approach to obtain information about ancestral population sizes, divergence times and migration rates from inferred genealogies at many neutrally evolving loci across the genome. We introduce new methods for accommodating gene flow between populations and integrating over possible phasings of diploid genotypes. We also describe a custom pipeline for genotype inference to mitigate biases from heterogeneous sequencing technologies and coverage levels. Our analysis indicates that the San population of southern Africa diverged from other human populations approximately 108–157 thousand years ago, that Eurasians diverged from an ancestral African population 38–64 thousand years ago, and that the effective population size of the ancestors of all modern humans was ~9,000.


September 16, 2011

Latent admixture causes spurious serial founder effect

There is a series of interesting papers on Amerindian populations in the early view section of the American Journal of Physical Anthropology. One of them struck my interest, because it deals with an issue that has been a familiar topos of this blog, and has, in my opinion, much greater potential applicability than the settlement of the Americas.

The basic idea of the paper is the following: the serial founder effect (SFE) is a model, whereby populations expand by successive splits, with daughter populations expanding and colonizing new territories. It is a tree model, with the nodes furthest from the root representing late founder populations, and the ones closest to the root representing early splits close (geographically and temporally) to the initial colonization impetus.

Gene identity is the probability that two random alleles from either two individuals in a population, or from two individuals from different populations will be identical. This has been used to argue for a SFE in the Americas, because it apparently matches expectations: the most basal populations are in north America, and gene identity increases toward south America.

However, the authors of the current paper show that the observed pattern is due to European admixture in native American populations; this makes the north American populations (that are more European-admixed and hence more different than the rest) appear both more basal and more diverse.

From the paper:
Many aspects of the pattern of neutral genetic variation in the Americas are consistent with the predictions of the serial founder effects process. The NJ tree is rooted in northern North America, it shows a northsouth pattern of internal branching, and gene identity within populations increases steadily with increasing geographic distance from Beringia. However, admixture with Europeans could account for all of these features. The tree is rooted in northern North America because the gene identities between the three northern North America populations and the other Native American populations are particularly low (Fig. 2). European admixture has contributed to this low identity, and, in principle, it could account for the position of the root. The Admixture tree (Fig. 5A) topology indicates that the north-south pattern of branching in the NJ tree might be the result of relatively high admixture in northern North America, intermediate levels in Central America and northern South America, and low levels in eastern South America. The partial correlation analyses show that the north-south increase in gene identity within populations can also be explained by geographically patterned admixture (Table 2). We conclude that geographically patterned admixture between Native Americans and Europeans has obscured our ability to reconstruct precontact evolutionary processes in the Americas.
Of course, this is an extremely important piece of work that future studies of Amerindian populations must take into account. It is no longer feasible to interpret the observed gene identity pattern in the Americas as a remnant of the migration and spread of Amerindian ancestors thousands of years ago. It is more likely a result of much more recent events, namely the different intensity of European admixture in post-1492 times.

Hunley and Healy is important not only for the Americas, however. The serial founder effect has been evoked to explain both the spread of modern humans from east Africa, as well as more recent Neolithic expansions in different parts of the world. We must now be vigilant that these patterns may, in part, be the result of latent admixture.

In the Americas, we know (from historical documents) that this admixture took place, and we have relatively unadmixed populations still in existence. But, there may very well have been admixture events before the birth of history, and many ancestral populations may no longer exist in unadmixed form. So, we may be interpreting patterns of modern human variation as the result of ancient colonization processes, oblivious to the presence of latent admixture.

For example, there is an increase in gene identity from eastern Africa through Arabia, and India, all the way to Siberia, and southward across the Americas. Hunley and Healy deal with the latter part of this cline, but the whole of it has been interpreted as evidence of an orderly Out of Africa colonization as a series of founder effects.

However, the Eurasian portion of the pattern may also be spurious: current east Africans, for example, are partially admixed, both with West Eurasians and with people from other parts of the continent. Likewise, Arabians often have African admixture, whereas South Asians have been convincingly shown to be largely 2-way mixes of West Eurasians and "Ancestral South Indians". To top it all off, we now have convincing evidence that archaic admixture may have played a role in the evolution of some living Africans: this would furthermore increase their gene diversity and contribute to a perceived Eurasian cline.

Tree models are orderly and well-behaved. It would be great if people behaved that way, because the math would be easier. But, people aren't laboratory mice that follow predefined paths in a maze: they mix with their neighbors, they split and move forward, but sometimes, they split and move backward. Hopefully, H&H's paper will lead to an increased appreciation of admixture in the human story, beyond the case of the Americas.

AJPA DOI: 10.1002/ajpa.21506

The Impact of Founder Effects, Gene Flow, and European Admixture on Native American Genetic Diversity

Keith Hunley and Meghan Healy

Recent studies have concluded that the global pattern of neutral genetic diversity in humans reflects a series of founder effects and population movements associated with our recent expansion out of Africa. In contrast, regional studies tend to emphasize the significance of more complex patterns of colonization, gene flow, and secondary population movements in shaping patterns of diversity. Our objective in this study is to examine how founder effects, gene flow, and European admixture have molded patterns of neutral genetic diversity in the Americas. Our strategy is to test the fit of a serial founder effects process to the pattern of neutral autosomal genetic variation and to examine the contribution of gene flow and European admixture to departures from fit. The genetic data consist of 678 autosomal microsatellite loci assayed by Wang and colleagues in 530 individuals in 29 widely distributed Native American populations. We find that previous evidence for serial founder effects in the Americas may be driven in part by high levels of European admixture in northern North America, intermediate levels in Central America, and low levels in eastern South America. Geographically patterned admixture may also account for previously reported genetic differences between Andean and Amazonian groups. Though admixture has obscured the precise details of precontact evolutionary processes, we find that genetic diversity is still largely hierarchically structured and that gene flow between neighboring groups has had surprisingly little impact on macrogeographic patterns of genetic diversity in the Americas.


Chris Stringer video on BBC on Iwo Eleru skulls

Skull points to a more complex human evolution in Africa
"[The skull] has got a much more primitive appearance, even though it is only 13,000 years old," said Chris Stringer, from London's Natural History Museum, who was part of the team of researchers.

"This suggests that human evolution in Africa was more complex... the transition to modern humans was not a straight transition and then a cut off."

Prof Stringer thinks that ancient humans did not die away once they had given rise to modern humans.

They may have continued to live alongside their descendants in Africa, perhaps exchanging genes with them, until more recently than had been thought.

The researchers say their findings also underscore a real lack of knowledge of human evolution in the region.

My previous blog post on the published article here.

A thing that has troubled me in reading a few recent palaeoanthropological comparative analyses is the fact that the Omo I, the "modern" of the ~195ka Omo skulls, as well as Herto do not seem to be included. Is this a case of anthropologists guarding their data, a problem that seems to have particularly plagued paleoanthropology? This is not an idle question: how would these ~200ka and ~150ka finds, widely touted as our ancestors fare when placed in the same analysis as the skulls of Harvati et al. (2011) or Mounier et al. (2011)?

Omo II, the most "archaic" of the Omo skulls was included in Mounier et al. (2011) and seemed to be related to Skhul 5 and Jebel Irhoud 1, which would probably place it in the intermediate (archaic/modern) category. How about Omo I?

I don't know, and I'd like to see some hard numbers on exactly how modern it is compared to extant humanity. It has often been repeated, for example, that the Skhul/Qafzeh hominins from the Levant represent an early Out-of-Africa movement, but they appear, at least in the latest Harvati et al. analysis to be well within the range of modern human variation, and certainly more so than all the included African samples of similar, or even younger age.

This seems counterintuitive: if, as the current orthodox theory holds, modern humans -in the strict sense of being like living people- originated in Africa ~200ka and spread to the rest of the world ~60ka, why are the Mt. Carmel hominins apparently more modern than their African counterparts of similar age? Remember, that it has been hypothesized that Skhul/Qafzeh represent a population that may be mixing with Eurasian Neandertals, which would make them less like modern people, not more.

Moreover, if modern humans did originate in Africa ~200ka, then why did they admix with archaic Africans only ~35ka (per Hammer et al. 2011) and had not replaced archaic Africans even ~13ka? Apparently, the current narrative proposes, they replaced all archaic hominins in Eurasia in practically a few thousands of years, but they could not achieve the same in nearly 0.2My in Africa? Or, they admixed with archaic Eurasians before they admixed with their next-door neighbors, the archaic Africans? Something does not seem right.

How would Omo I and Herto fare if they had been included? Ancestral H. s. sapiens, where art thou? Let's find out.

16-12 ka humans with archaic features from Iwo Eleru, Nigeria

This is a nice physical anthropological complement to the recent Hammer et al. paper on archaic admixture in Africans. It is also added to a growing list of late survivals in the African palaeoanthropological record with apparent archaic features.

As I have mentioned before, people have been too quick to generalize about "modern humans in Africa" from the early anatomically modern humans of eastern Africa, forgetting that our focus on them has been an artifact of the good geological conditions for preservation in that area, and the resulting overwhelming scientific interest in the region.

But, eastern Africa is the periphery of Sub-Saharan Africa, and we are lucky to have new finds described from West Africa and elsewhere, as in this paper.

I bet that a few years from now, we will look with amazement at the naivete of the passing Out of Africa orthodoxy that bundled all Africans into an amorphous category of "our ancestors in Africa". It is also becoming clearer that increased African genetic variation is, at least in part, due to the continent being home to multiple deeply divergent populations that persisted, in various admixtures down to the present.

The PCA and CVA results are quite instructive:
Symbols: Grey diamonds. Modern humans; Black up triangles: Upper Paleolithic modern humans; Purple up triangles: Late Pleistocene African and Near Eastern hominins; Red stars: H. neanderthalensis; Red squares: H. heidelbergensis (s.l.); Black squares: H. erectus (s.l.). Ellipses indicate 95% confidence ellipses for Neanderthals (red) and modern humans (gray).
From the paper:
Modern human populations were characterized by more positive scores on PC 1, and there was only minimal overlap among their 95% confidence ellipses and that of the Neanderthals. The Middle-Late Pleistocene African specimens (LH 18, Singa, Djebel Irhoud 1 and 2) and the early modern human specimens from Qafzeh and Skhul fell in the intermediate zone between Neanderthals / H. heidelbergensis on one hand and modern humans on the other. Qafzeh 9 was the exception, falling on the positive end of PC 1 and close to Upper Paleolithic European specimens. The latter sample, which included some of the earliest modern human specimens in Europe (Mladec 1 and 5, Oase 2, Muierii 1, Cioclovina), clustered within the modern human range of variation, and not in the zone of overlap with the archaic specimens.
Note a few things:
  • the similarity of Qafzeh 9 with Upper Paleolithic Europeans; geneticists had better stop inferring that the Skhul/Qafzeh hominids were the "first Out-of-Africa that failed"
  • the similarity of Qafzeh 6 with Upper Cave 1 from Zhoukoudian.
If you have Qz9 and Qz6, i.e., more than 100,000 year old West Asian skulls clustering with Upper Paleolithic Europeans and East Asians, it is becoming increasingly difficult to maintain the naive Out-of-Africa orthodoxy that a recent Out-of-Africa push as late as 60,000 years is responsible for the peopling of Eurasia.

This is especially the case when Qafzeh 9 may be the earliest unambiguously modern human with no "ifs and buts", with Skhul and Qz6 following close behind.

In the conclusion of their paper, the authors mention another skull with archaic features, from Congo:
Thus our restudy of the Iwo Eleru cranium confirms previously noted archaic cranial shape aspects, and the U-series age estimates on its skeleton support the previously proposed terminal Pleistocene date for this burial. Our findings also support suggestions of deep population substructure in Africa and a complex evolutionary process for the origin of modern humans [16], [17], [7], [18], [19], [20], [21]. Perhaps most importantly, our analysis highlights the dearth of hominin finds from West Africa, and underscores our real lack of knowledge of human evolution in that region, as well as others. As also indicated by restudy of the Ishango (Congo) fossils [22], Later Stone Age fossils from at least two regions of Africa retain significant archaic aspects in their skeletons. We hope that the next stage of this research will extend studies to the Iwo Eleru mandible and postcrania, and to comparative materials such as those from Ishango.
According to paper co-author Chris Stringer:
Hi Dienekes, Unfortunately PLoS introduced a typo in the summary regarding the date, which should have read ~11.7–16.3 ka. Everyone please bear in mind the analysis only covered the superior cranial vault, as there was no face - I discuss the results further in my new book The Origin of Our Species.
UPDATE: Chris Stringer video and more thoughts

PLoS ONE 6(9): e24024. doi:10.1371/journal.pone.0024024

The Later Stone Age Calvaria from Iwo Eleru, Nigeria: Morphology and Chronology

Katerina Harvati et al.

In recent years the Later Stone Age has been redated to a much deeper time depth than previously thought. At the same time, human remains from this time period are scarce in Africa, and even rarer in West Africa. The Iwo Eleru burial is one of the few human skeletal remains associated with Later Stone Age artifacts in that region with a proposed Pleistocene date. We undertook a morphometric reanalysis of this cranium in order to better assess its affinities. We also conducted Uranium-series dating to re-evaluate its chronology.

Methodology/Principal Findings
A 3-D geometric morphometric analysis of cranial landmarks and semilandmarks was conducted using a large comparative fossil and modern human sample. The measurements were collected in the form of three dimensional coordinates and processed using Generalized Procrustes Analysis. Principal components, canonical variates, Mahalanobis D2 and Procrustes distance analyses were performed. The results were further visualized by comparing specimen and mean configurations. Results point to a morphological similarity with late archaic African specimens dating to the Late Pleistocene. A long bone cortical fragment was made available for U-series analysis in order to re-date the specimen. The results (~11.7–6.3 ka) support a terminal Pleistocene chronology for the Iwo Eleru burial as was also suggested by the original radiocarbon dating results and by stratigraphic evidence.

Our findings are in accordance with suggestions of deep population substructure in Africa and a complex evolutionary process for the origin of modern humans. They further highlight the dearth of hominin finds from West Africa, and underscore our real lack of knowledge of human evolution in that region.


September 15, 2011

Ötzi, the Tyrolean Iceman belonged to Y-haplogroup G2a4

G was the third most popular choice in my recent poll.

We now have G2a3 from Neolithic Linearbandkeramik in Derenburg and G2a in Treilles in addition to Ötzi from the Alps. G2a folk got around. He joins Stalin and Louis XVI as a famous G2a.

It was already clear with the discovery of G2a in France and Central Europe, that this otherwise uncommon present-day haplogroup in Europe was more prominent during the Neolithic, and Ötzi's data point seals the case.

In a sense, the triple G2a finds in Neolithic Europe confirm the origins of the European Neolithic population in West Asia, but renew the mystery as to how all the rest of the "players" of the European Y-DNA scene appeared on the scene, with everything except G and I first appearing in the ancient DNA record after the end of the Neolithic.

Ötzi has been added to the ancient Y-chromosome studies page.

September 14, 2011

The Caucasus revisited (Yunusbayev et al. 2011)

This is another treasure trove of a paper, and together with Balanovsky et al. (2011) we now have a very clear picture of genetic variation in this most interesting of world regions.

Here is the ADMIXTURE analysis:

The authors also post results up to K=10 in the supplementary material, which show Druze/Bedouin/Basque-centered component. It is actually possible to push the analysis higher than K=7 without such problem components appearing, by retaining non-closely related individuals (using --genome in PLINK and then iteratively removing individuals from pairs with PI_HAT greater than some value).

Nonetheless, the components emerging from this analysis will be familiar to followers of the Dodecad Project. In terms of Dodecad v3:
  • light yellow "North East Asian"
  • orange "South East Asian"
  • brown "Neo African" or "Sub_Saharan", as there are no African hunter-gatherers
  • dark blue "North European", as there is no split of east/west Europe at this level
  • middle blue "West Asian"
  • light blue "Southwest Asian"
  • green "South Asian", but anchored on Sindhi, a population from Pakistan, due to the lack of more southern populations from India
The labels of new populations sampled in this study can be seen in brown. I particularly hope that the substantial new autosomal data will become publicly available, so that I can use them in the Dodecad Project. It will be an invaluable new resource, filling some "holes" in the Eurasian landscape (e.g., east of the Caspian; Bulgarians; several new Caucasus populations) in the Li et al. (HGDP), and Behar et al. data.

(to be continued)

UPDATE I (Y-chromosomes):

Some observations:
  • C has a concentration in the Turkic Nogays
  • The presence of D this far west is very surprising, again in the Nogays. This haplogroup has a relic distribution, with particular concentrations in Tibet, Mongolia, Japan, and Andaman Islanders. In all likelihood its presence here is linked to the Nogays' eastern origin
  • E and its subclades occurs at a very low frequency here
  • G2a has a clear West Caucasus (both north and south) concentration
  • I seems to have a mainly West Caucasus distribution as well; this is a common European haplogroup; it has quite elevated frequencies among the Andis and Kara Nogays. It would be interesting to discover some historical correlate for the presence of I in Kara Nogays but not Kuban Nogays and in Andis but not in most of the NE Caucasus
  • J1 has the expected Northeast Caucasus nexus. This haplogroup is bimodal, with a mode in Arabians and a secondary mode in NE Caucasus. Note the paucity of J1e-P58, the reverse of the situation of Arabians; I've noted before the likely association of the P58 clade with Semitic languages.
  • The extreme concentration of J2 in Chechens and Ingush are probably associated with low variance. Apart from these atypical populations, a substantial presence of this haplogroup can be found in the NW/S Caucasus in different populations and in the form of different subclades.
  • The new LT mystery clade has its usual low-frequency wide distribution
  • N occurs in Nogays as expected, and, like C, also in the NW Caucasus. This probably also represents an eastern influence, probably associated not only with the Nogays but also with various Tatar influences on the Caucasus.
  • Q occurs widely in the NW Caucasus but only in 1 Nogay. Perhaps this is more of a Tatar marker, although a finer-scale resolution of this haplogroup is really necessary.
  • R1a-related lineages occur less frequently here among eastern Slavs, a main reason for the disconnect between the Eastern European plain and the Caucasus. There does, however, appear to be good diversity here, with the presence of R1a*, R1a1-M198*, Note again how the Iranic Ossetians (both North and South) have almost no R1a1 compared to both their NW Caucasian and S Caucasian neighbors, again, suggesting that this may not have been an important Alan or steppe Iranian lineage, at least during the late antique time horizon. The occurrence of R1a1f-M458 may represent Slavic influence in the NW Caucasus.
  • R1b-related lineages seem ubuiquitous in the Caucasus. R-M73 occurs substantially in Kara Nogays and Balkars, an apparent link with Central Asia where this haplogroup occurs frequently.
UPDATE II (Caucasus-Eastern Europe discontinuity)

The authors of this paper highlight the genetic discontinuity between the eastern European plain and the Caucasus. This was also apparent in the Balanovsky et al. (2011) paper, and was also a major conclusion of the Dodecad Project, with Caucasians exhibiting a high percentage of the "West Asian" component, while eastern Slavs low "West Asian" and high "East European".

The interpretation of this discontinuity is more difficult. There are surely parts of the Caucasus region that are mountainous and pose an ecological contrast to the flatlands of eastern Europe. That is consistent with a different type of population living in either region for a long time, despite the well-attested archaological contacts (e.g., Maikop or the settlement of steppe nomads such as Alans or Sarmatians).

On the other hand, the eastern Slavic population can, at least in part, have expanded more recently, in the medieval period, as part of the early Slavic dispersals, as well as the push to the north and east of the Russians. These appear to have partly displaced Turkic groups from the north Pontic region, with all of the above having displaced historical Scythian (Iranic) nomads, who, in turn, displaced the mysterious Cimmerians. If the discovery of east Eurasian mtDNA C in Neolithic and Bronze Age Ukraine stands up, there will be another layer of population replacement, as mtDNA C is quite rare in the broader region today. On the other hand, the Caucasus itself may have been affected from population movements from the Near East, as Balanovsky et al. suggest.

So, in conclusion, the discontinuity is a fact that emerges from different types of analyses, but its causes remain uncertain, and it is not clear when and how it was first established.

Mol Biol Evol (2011) doi: 10.1093/molbev/msr221

The Caucasus as an asymmetric semipermeable barrier to ancient human migrations

Bayazit Yunusbayev et al.


The Caucasus, inhabited by modern humans since the Early Upper Paleolithic and known for its linguistic diversity, is considered to be important for understanding human dispersals and genetic diversity in Eurasia. We report a synthesis of autosomal, Y chromosome and mitochondrial DNA (mtDNA) variation in populations from all major subregions and linguistic phyla of the area. Autosomal genome variation in the Caucasus reveals significant genetic uniformity among its ethnically and linguistically diverse populations, and is consistent with predominantly Near/Middle Eastern origin of the Caucasians, with minor external impacts. In contrast to autosomal and mtDNA variation, signals of regional Y chromosome founder effects distinguish the eastern from western North Caucasians. Genetic discontinuity between the North Caucasus and the East European Plain contrasts with continuity through Anatolia and the Balkans, suggesting major routes of ancient gene flows and admixture.


September 13, 2011

Strong isolation between Neandertals and modern humans

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:
  1. Why Chinese don't have less Neandertal admixture than Europeans, even though Neandertals were a West Eurasian distributed species
  2. Why no Neandertal mtDNA is detected in modern samples
I will begin with #2, which is tangential to the paper's overall simulation framework. The authors write:
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.
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.

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:
  1. 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
  2. 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
  3. 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
In any case, the C&E paper is an important contribution to the emerging new debate about human origins. The central prediction of their model, that modern human/Neandertal admixture was no easy thing is certainly consistent with everything we know about human behavior. Homogamy seems to be a tendency of our species, and heterogamy between populations separated by hundreds of thousands of years of separate evolution cannot have been frequent.

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 have
two comments on your main concerns:

1) You seem to conclude that our model assumes that Chinese only followed a
northern route, but what we portray in our Figure 3 is a map representing
introgression event densities, which does not necessarily represent the
migrations followed by the ancestors of Chinese people. In our simulations,
migrants could indeed go South of the Himalaya, but since we assumed there
were 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 migration
routes to Asia, Asian populations having interacted with Neanderthals for
about the same amount of time (or in space) would have about the same final
level of introgression. So we would not (and never did) say that East Asian
have followed a migration route North of the Himalayas.

2) Concerning you big elephant, we indeed believe that current Europeans are
mainly descending from Paleolithic people, and we have a specific paper on
this (Currat M, Excoffier L (2005) The effect of the Neolithic expansion on
European molecular diversity. Proceedings of the Royal Society London B 272,
679-688), and a later paper examining and explaining why local genes are likely
to massively introgress the genome of populations invading the territory of
a local species (Currat M, Ruedi M, Petit RJ, Excoffier L (2008) The
hidden side of invasions: Massive introgression by local genes. Evolution
62, 1908-1920). It thus appears very likely to us that the Paleolithic gene
pool of Europeans has largely persisted in modern humans, despite posterior
Neolithic migrations, if we assume that Neolithic populations mixed to some
appreciable extent with local paleolithics during their expansion over

Anyway, it is good that our paper promotes discussions on the dynamics of
the settlement, and that spatial aspects of human evolution are now given
some importance.


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:
  • 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.
The issue can only be settled, of course, if we are ever lucky enough to obtain ancient DNA from Upper Paleolithic Europeans.

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.