Mungo Man DNA revisited + first ancient mtDNA from Australia

The authors find that previously published mtDNA from earliest Australians was contamination, and one S2 mtDNA haplogroup in an undated sample of likely Holocene origin.

PNAS doi: 10.1073/pnas.1521066113

Ancient mtDNA sequences from the First Australians revisited

Tim H. Heupink et al.

The publication in 2001 by Adcock et al. [Adcock GJ, et al. (2001) Proc Natl Acad Sci USA 98(2):537–542] in PNAS reported the recovery of short mtDNA sequences from ancient Australians, including the 42,000-y-old Mungo Man [Willandra Lakes Hominid (WLH3)]. This landmark study in human ancient DNA suggested that an early modern human mitochondrial lineage emerged in Asia and that the theory of modern human origins could no longer be considered solely through the lens of the “Out of Africa” model. To evaluate these claims, we used second generation DNA sequencing and capture methods as well as PCR-based and single-primer extension (SPEX) approaches to reexamine the same four Willandra Lakes and Kow Swamp 8 (KS8) remains studied in the work by Adcock et al. Two of the remains sampled contained no identifiable human DNA (WLH15 and WLH55), whereas the Mungo Man (WLH3) sample contained no Aboriginal Australian DNA. KS8 reveals human mitochondrial sequences that differ from the previously inferred sequence. Instead, we recover a total of five modern European contaminants from Mungo Man (WLH3). We show that the remaining sample (WLH4) contains ∼1.4% human DNA, from which we assembled two complete mitochondrial genomes. One of these was a previously unidentified Aboriginal Australian haplotype belonging to haplogroup S2 that we sequenced to a high coverage. The other was a contaminating modern European mitochondrial haplotype. Although none of the sequences that we recovered matched those reported by Adcock et al., except a contaminant, these findings show the feasibility of obtaining important information from ancient Aboriginal Australian remains.

Link

No Y-chromosomes of recent Indian origin in Australians

Current Biology http://dx.doi.org/10.1016/j.cub.2016.01.028

Deep Roots for Aboriginal Australian Y Chromosomes

Anders Bergström et al.

Australia was one of the earliest regions outside Africa to be colonized by fully modern humans, with archaeological evidence for human presence by 47,000 years ago (47 kya) widely accepted [ 1, 2 ]. However, the extent of subsequent human entry before the European colonial age is less clear. The dingo reached Australia about 4 kya, indirectly implying human contact, which some have linked to changes in language and stone tool technology to suggest substantial cultural changes at the same time [ 3 ]. Genetic data of two kinds have been proposed to support gene flow from the Indian subcontinent to Australia at this time, as well: first, signs of South Asian admixture in Aboriginal Australian genomes have been reported on the basis of genome-wide SNP data [ 4 ]; and second, a Y chromosome lineage designated haplogroup C∗, present in both India and Australia, was estimated to have a most recent common ancestor around 5 kya and to have entered Australia from India [ 5 ]. Here, we sequence 13 Aboriginal Australian Y chromosomes to re-investigate their divergence times from Y chromosomes in other continents, including a comparison of Aboriginal Australian and South Asian haplogroup C chromosomes. We find divergence times dating back to ∼50 kya, thus excluding the Y chromosome as providing evidence for recent gene flow from India into Australia.

Link

Paleoamericans galore

Two new papers in Nature and Science add to the debate on Native American origins. The first study (in Nature) detects that some Amazonians have a few percent ancestry from a group related to Australasians, which suggests that early native Americans were not homogeneous but came in two flavors: the main one found all over the Americans and the Australasian-related one. The second study (in Science) looks at ancient "Paleoamerican"-postulated populations and finds that they don't have any particular relationship to Australasians. Thus, whatever population brought the "Paleoamerican" admixture into the Amazon, it remains to be found.

Nature (2015) doi:10.1038/nature14895

Genetic evidence for two founding populations of the Americas 

Pontus Skoglund et al.

Genetic studies have consistently indicated a single common origin of Native American groups from Central and South America1, 2, 3, 4. However, some morphological studies have suggested a more complex picture, whereby the northeast Asian affinities of present-day Native Americans contrast with a distinctive morphology seen in some of the earliest American skeletons, which share traits with present-day Australasians (indigenous groups in Australia, Melanesia, and island Southeast Asia)5, 6, 7, 8. Here we analyse genome-wide data to show that some Amazonian Native Americans descend partly from a Native American founding population that carried ancestry more closely related to indigenous Australians, New Guineans and Andaman Islanders than to any present-day Eurasians or Native Americans. This signature is not present to the same extent, or at all, in present-day Northern and Central Americans or in a ~12,600-year-old Clovis-associated genome, suggesting a more diverse set of founding populations of the Americas than previously accepted.

Link

Science DOI: 10.1126/science.aab3884

Genomic evidence for the Pleistocene and recent population history of Native Americans

Maanasa Raghavan1,*, Matthias Steinrücken2,3,4,*, Kelley Harris5,*, Stephan Schiffels6,*, Simon Rasmussen7,*, Michael DeGiorgio8,*, Anders Albrechtsen9,*, Cristina Valdiosera1,10,*, María C. Ávila-Arcos1,11,*, Anna-Sapfo Malaspinas1* et al.

How and when the Americas were populated remains contentious. Using ancient and modern genome-wide data, we find that the ancestors of all present-day Native Americans, including Athabascans and Amerindians, entered the Americas as a single migration wave from Siberia no earlier than 23 thousand years ago (KYA), and after no more than 8,000-year isolation period in Beringia. Following their arrival to the Americas, ancestral Native Americans diversified into two basal genetic branches around 13 KYA, one that is now dispersed across North and South America and the other is restricted to North America. Subsequent gene flow resulted in some Native Americans sharing ancestry with present-day East Asians (including Siberians) and, more distantly, Australo-Melanesians. Putative ‘Paleoamerican’ relict populations, including the historical Mexican Pericúes and South American Fuego-Patagonians, are not directly related to modern Australo-Melanesians as suggested by the Paleoamerican Model.

Link

In search of the source of Denisovan ancestry

bioRxiv http://dx.doi.org/10.1101/017475

Denisovan Ancestry in East Eurasian and Native American Populations.

Pengfei Qin , Mark Stoneking

Although initial studies suggested that Denisovan ancestry was found only in modern human populations from island Southeast Asia and Oceania, more recent studies have suggested that Denisovan ancestry may be more widespread. However, the geographic extent of Denisovan ancestry has not been determined, and moreover the relationship between the Denisovan ancestry in Oceania and that elsewhere has not been studied. Here we analyze genome-wide SNP data from 2493 individuals from 221 worldwide populations, and show that there is a widespread signal of a very low level of Denisovan ancestry across Eastern Eurasian and Native American (EE/NA) populations. We also verify a higher level of Denisovan ancestry in Oceania than that in EE/NA; the Denisovan ancestry in Oceania is correlated with the amount of New Guinea ancestry, but not the amount of Australian ancestry, indicating that recent gene flow from New Guinea likely accounts for signals of Denisovan ancestry across Oceania. However, Denisovan ancestry in EE/NA populations is equally correlated with their New Guinea or their Australian ancestry, suggesting a common source for the Denisovan ancestry in EE/NA and Oceanian populations. Our results suggest that Denisovan ancestry in EE/NA is derived either from common ancestry with, or gene flow from, the common ancestor of New Guineans and Australians, indicating a more complex history involving East Eurasians and Oceanians than previously suspected.

Link

Genetic evidence for the colonization of Australia

Quaternary International Volume 285, 8 February 2013, Pages 44–56

Genetic evidence for the colonization of Australia

Sheila van Holst Pellekaan et al.

Mitochondrial DNA (mtDNA), Y-chromosome and, more recently, genome studies from living people have produced powerful evidence for the dispersal of modern human populations. The prevailing model of global dispersion assumes an African origin in which Australia and the American continents represent some of the extreme regions of human migration, though the relative timing of dispersal events remains debatable. Here, a focus on Australia and New Guinea discusses currently available genetic evidence from the two regions, compared with that from Asia. Mt haplotypes indicate ancient ancestry for both Australia and New Guinea peoples, with evidence of some shared genetic connection and other unshared haplogroups apparently specific to both places. Migration into Sahul from south-east Asia may have been by more complex routes than only along a ‘southern coastal route’, raising the question of possible common ancestry in central or northern Asia for some Australian and American peoples for which current genetic evidence is tenuous. Although current dating methods for genetic diversity rely heavily on several assumptions, best estimates provide support for archaeological dates, indicating that, relative to the colonization of America, Australia was inhabited very early. Genetic diversity of living descendants of Australia’s founding populations is informative for dispersal within Australia and for understanding complex population histories of Asia.

Link

Gene flow between Indian populations and Australasia ~4,000 years ago

Only the press release is available so far, I will add the paper abstract when I see it on the PNAS website:

Researcher Irina Pugach and colleagues now analysed genetic variation from across the genome from aboriginal Australians, New Guineans, island Southeast Asians, and Indians. Their findings suggest substantial gene flow from India to Australia 4,230 years ago. i.e. during the Holocene and well before European contact. “Interestingly,” says Pugach, “this date also coincides with many changes in the archaeological record of Australia, which include a sudden change in plant processing and stone tool technologies, with microliths appearing for the first time, and the first appearance of the dingo in the fossil record. Since we detect inflow of genes from India into Australia at around the same time, it is likely that these changes were related to this migration.” 

Their analyses also reveal a common origin for populations from Australia, New Guinea and the Mamanwa – a Negrito group from the Philippines – and they estimated that these groups split from each other about 36,000 years ago. Mark Stoneking says: “This finding supports the view that these populations represent the descendants of an early ‘southern route’ migration out of Africa, while other populations in the region arrived later by a separate dispersal.“ This also indicates that Australians and New Guineans diverged early in the history of Sahul, and not when the lands were separated by rising sea waters around 8,000 years ago.

A relationship between Indian and Australasian populations has long been suspected on various grounds (e.g., HGDP Papuans often show membership in a "South Asian" ancestral component at low levels of resolution). It will be interesting to see the model proposed in the new paper about the admixture event leading to modern Australasians.

UPDATE: Ed Yong covers the story in Nature News:

Some aboriginal Australians can trace as much as 11% of their genomes to migrants who reached the island around 4,000 years ago from India, a study suggests. Along with their genes, the migrants brought different tool-making techniques and the ancestors of the dingo, researchers say1.

From World News Australia:

The study suggests that in addition to an earlier northern route of migration out of Africa, into Asia, and then South East Asia about 60,000 to 70,000 years ago, the second wave occurred much later, arriving during the Holocene period about 4,230 years ago.
...
“About that point in the archaeological record, there were significant changes in the use of stone tools, in hunting techniques and significantly, the introduction of the dingo,” Professor Cooper said.
...
There are other theories that may support the evidence of a more recent influx of migrants from India, including that they brought with them a disease of epidemic proportions that wiped out earlier Aboriginal populations.

UPDATE II: I added the abstract.

PNAS doi: 10.1073/pnas.1211927110

Genome-wide data substantiate Holocene gene flow from India to Australia 

Irina Pugach et al.

The Australian continent holds some of the earliest archaeological evidence for the expansion of modern humans out of Africa, with initial occupation at least 40,000 y ago. It is commonly assumed that Australia remained largely isolated following initial colonization, but the genetic history of Australians has not been explored in detail to address this issue. Here, we analyze large-scale genotyping data from aboriginal Australians, New Guineans, island Southeast Asians and Indians. We find an ancient association between Australia, New Guinea, and the Mamanwa (a Negrito group from the Philippines), with divergence times for these groups estimated at 36,000 y ago, and supporting the view that these populations represent the descendants of an early “southern route” migration out of Africa, whereas other populations in the region arrived later by a separate dispersal. We also detect a signal indicative of substantial gene flow between the Indian populations and Australia well before European contact, contrary to the prevailing view that there was no contact between Australia and the rest of the world. We estimate this gene flow to have occurred during the Holocene, 4,230 y ago. This is also approximately when changes in tool technology, food processing, and the dingo appear in the Australian archaeological record, suggesting that these may be related to the migration from India.

Link

Major new ancient DNA project on Southeast Asia and Australia

It seems that I read about a new major project on ancient DNA every other day. There is a lot of activity in this field, which will, no doubt, bear fruit in the coming years.

What I really want to see is a complete genome sequence of early Homo sapiens, e.g., from a sample about as old as Vindija and Denisova. If anyone knows of any such sequencing efforts in the works, write in the comments, or drop me an e-mail.

DNA analysis of ancient remains to uncover origin mysteries
Griffith University leads search for human evolution

In collaboration with the Universities of Auckland, Copenhagen and New South Wales, the researchers will analyse human remains from continental and oceanic Asia and Australia using more powerful newly developed ancient DNA sequencing methods.
Chief Investigator Professor David Lambert from the School of Environment says understanding where the earliest people of Asia and continental Australia came from is critical to understanding modern human evolution.

"The recent sequencing of the Australian Aboriginal genome has identified two waves of human migration through Asia,'' he said.

"Aboriginal Australians descended from 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, although there is evidence for hybridisation between them."

The researchers aim to identify descendent individuals from both lineages and detect historic patterns of interbreeding among these early people.

Professor Paul Tacon from Griffith University's Place, Evolution & Rock Art Heritage Unit said the research was a world-first study to attempt to recover human DNA sequences from more than 80 ancient human remains collected from a range of time points.
"We aim to identify the mitochondrial DNA lineage of each sample of human remains, the migration wave they represented and evidence of biological interactions, such as hybridisation with other groups.

"Although complete or draft genomes have been recovered from extinct species such as Neandertals and Woolly Mammoths, there are no existing populations of these species available for comparison.

"But an increasing number of complete human genomes in our study provide the foundation for this work."

Professor Tacon said the study was possible because of recent advances in second-generation DNA sequencing and parallel developments in DNA target capture technologies.

"These developments provide extraordinary new possibilities in the field of ancient human genomics."

The study is part of a $550,000 three-year Australian Research Council Linkage Grant.

Y-chromosome admixture in self-identified Australian Aboriginals

Forensic Sci Int Genet. 2012 Jan 30. [Epub ahead of print]

An investigation of admixture in an Australian Aboriginal Y-chromosome STR database.

Taylor D, Nagle N, Ballantyne KN, van Oorschot RA, Wilcox S, Henry J, Turakulov R, Mitchell RJ.

Abstract

Y-chromosome specific STR profiling is increasingly used in forensic casework. However, the strong geographic clustering of Y haplogroups can lead to large differences in Y-STR haplotype frequencies between different ethnicities, which may have an impact on database composition in admixed populations. Aboriginal people have inhabited Australia for over 40,000 years and until ∼300 years ago they lived in almost complete isolation. Since the late 18th century Australia has experienced massive immigration, mainly from Europe, although in recent times from more widespread origins. This colonisation resulted in highly asymmetrical admixture between the immigrants and the indigenes. A State jurisdiction within Australia has created an Aboriginal Y-STR database in which assignment of ethnicity was by self-declaration. This criterion means that some males who identify culturally as members of a particular ethnic group may have a Y haplogroup characteristic of another ethnic group, as a result of admixture in their paternal line. As this may be frequent in Australia, an examination of the extent of genetic admixture within the database was performed. A Y haplogroup predictor program was first used to identify Y haplotypes that could be assigned to a European haplogroup. Of the 757 males (589 unique haplotypes), 445 (58.8%) were identified as European (354 haplotypes). The 312 non-assigned males (235 haplotypes) were then typed, in a hierarchical fashion, with a Y-SNP panel that detected the major Y haplogroups, C-S, as well as the Aboriginal subgroup of C, C4. Among these 96 males were found to have non-Aboriginal haplogroups. In total, ∼70% of Y chromosomes in the Aboriginal database could be classed as non-indigenous, with only 169 (129 unique haplotypes) or 22% of the total being associated with haplogroups denoting Aboriginal ancestry, C4 and K* or more correctly K(xL,M,N,O,P,Q,R,S). The relative frequencies of these indigenous haplogroups in South Australia (S.A.) were significantly different to those seen in samples from the Northern Territory and Western Australia. In S.A., K* (∼60%) has a much higher frequency than C4 (∼40%), and the subgroup of C4, C4(DYS390.1del), comprised only 17%. Clearly admixture in the paternal line is at high levels among males who identify themselves as Australian Aboriginals and this knowledge may have implications for the compilation and use of Y-STR databases in frequency estimates.

Link

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...

More:

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"?

More:

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.

More:

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?

More:

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
   

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.

Abstract

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.

Link

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.

ABSTRACT

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.

Link

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
doi:10.1016/j.ajhg.2011.09.005

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.

Link

Y-chromosomes of Filipino Negritos and non-Negritos

European Journal of Human Genetics (29 September 2010) | doi:10.1038/ejhg.2010.162

The Y-chromosome landscape of the Philippines: extensive heterogeneity and varying genetic affinities of Negrito and non-Negrito groups

Frederick Delfin et al.


The Philippines exhibits a rich diversity of people, languages, and culture, including so-called ‘Negrito’ groups that have for long fascinated anthropologists, yet little is known about their genetic diversity. We report here, a survey of Y-chromosome variation in 390 individuals from 16 Filipino ethnolinguistic groups, including six Negrito groups, from across the archipelago. We find extreme diversity in the Y-chromosome lineages of Filipino groups with heterogeneity seen in both Negrito and non-Negrito groups, which does not support a simple dichotomy of Filipino groups as Negrito vs non-Negrito. Filipino non-recombining region of the human Y chromosome lineages reflect a chronology that extends from after the initial colonization of the Asia-Pacific region, to the time frame of the Austronesian expansion. Filipino groups appear to have diverse genetic affinities with different populations in the Asia-Pacific region. In particular, some Negrito groups are associated with indigenous Australians, with a potential time for the association ranging from the initial colonization of the region to more recent (after colonization) times. Overall, our results indicate extensive heterogeneity contributing to a complex genetic history for Filipino groups, with varying roles for migrations from outside the Philippines, genetic drift, and admixture among neighboring groups.

Link

A rare genomic look at Aboriginal Australians

How strange that modern genetics is supposed to have invalidated the concept of race, yet, at every turn, it confirms most of the basic racial taxonomic observations of people working only with their eyes and, much later, their calipers.

On the left is the frappe analysis from the supplementary material, the Oceanian populations are seen on the far right.

The Australasid cluster emerges as an entity at K=5, showing Caucasoid admixture (AUR), Mongoloid admixture (MEL), and no apparent admixture (PAP).

At K=8 it is evident that the Caucasoid admixture in Aboriginal Australians is specifically European in origin, certainly the result of colonization in very recent times.

What can account for the Mongoloid admixture in Melanesians? It is probably the recent spread of Austronesian languages, arguably the most epic maritime language spread before Columbus, which affected a good deal of the southern hemisphere from Madagascar through Indonesia, Micronesia, Melanesia, and all the way to Polynesia on the far end.

As for the unadmixed Papuans, the indigenous inhabitants of New Guinea, their results are not surprising: there is a lack of admixture of East Asian Y chromosomes on the island, even in its most affected NW corner (Bird's head) where this admixture runs only to about 2.5%.

The American Journal of Human Genetics, doi:10.1016/j.ajhg.2010.07.008

Whole-Genome Genetic Diversity in a Sample of Australians with Deep Aboriginal Ancestry

Brian P. McEvoy et al.

Australia was probably settled soon after modern humans left Africa, but details of this ancient migration are not well understood. Debate centers on whether the Pleistocene Sahul continent (composed of New Guinea, Australia, and Tasmania) was first settled by a single wave followed by regional divergence into Aboriginal Australian and New Guinean populations (common origin) or whether different parts of the continent were initially populated independently. Australia has been the subject of relatively few DNA studies even though understanding regional variation in genomic structure and diversity will be important if disease-association mapping methods are to be successfully evaluated and applied across populations. We report on a genome-wide investigation of Australian Aboriginal SNP diversity in a sample of participants from the Riverine region. The phylogenetic relationship of these Aboriginal Australians to a range of other global populations demonstrates a deep common origin with Papuan New Guineans and Melanesians, with little evidence of substantial later migration until the very recent arrival of European colonists. The study provides valuable and robust insights into an early and important phase of human colonization of the globe. A broader survey of Australia, including diverse geographic sample populations, will be required to fully appreciate the continent's unique population history and consequent genetic heritage, as well as the importance of both to the understanding of health issues.

Link

Origin and dispersal of Y chromosome haplogroup C (Zhong et al. 2010)

A beautiful new paper has appeared that tackles the distribution and substructure of Y chromosome haplogroup C, a widely dispersed lineage that binds Asia, Oceania, and the Americas. This will be invaluable as a resource for students of East Eurasian anthropology and genetics. My only problem with the paper is in its use of the evolutionary mutation rate that I have criticized elsewhere.

From the paper:

Hg C is prevalent in various geographical areas (Figures 1 and 2), including Australia (65.74%), Polynesia (40.52%), Heilongjiang of northeastern China (Manchu, 44.00%), Inner Mongolia (Mongolian, 52.17%; Oroqen, 61.29%), Xinjiang of northwestern China (Hazak, 75.47%), Outer Mongolia (52.80%) and northeastern Siberia (37.41%). Hg C is also present in other regions, extending longitudinally from Sardinia in Southern Europe all the way to Northern Colombia, and latitudinally from Yakutia of Northern Siberia and Alaska of Northern America to India, Indonesia and Polynesia, but absent in Africa.

On the structure of haplogroup C:

As shown in Figure 1, most of the subhaplogroups of Hg C have a geographically pronounced distribution. Hg C6, which is defined by a recently identified marker, was not detected in our samples. Hg C1 and C4 are completely restricted to Japan and Australia, respectively, and not detected in the other samples from East Asia and Southeast Asia. Hg C5 occurs in India and its neighboring regions Pakistan and Nepal. In mainland East Asia, four Hg C5 individuals were detected, including two in Xibe, one in Uygur and one in Shanxi Han. Although the dispersal of Hg C2 is relatively wide, its distribution remains limited to Oceania and its neighboring regions, except Australia. In our samples, only three Hg C2 individuals were observed in Eastern Indonesia, which is consistent with previous reports. Hg C3 is the most widespread subhaplogroup, which was detected in Central Asia, South Asia, Southeast Asia, East Asia, Siberia and the Americas, but absent in Oceania. Different subhaplogroups of Hg C that do not overlap between the regions suggest that these individuals have undergone long-time isolation. As these subhaplogroups have a common origin by sharing the M130-derived allele, their geographical distributions enable us to infer the prehistoric migration routes of this lineage.

The MDS plot is quite instructive. Notice the duality of Japanese C chromosomes, which parallels what we know about the dual origins of the Japanese. It would be instructive to test European haplogroup C outliers to see where they fall within haplogroup C diversity.

The C3 MDS is quite instructive, and shows quite well the distribution of C3 diversity in Chinese ethnic populations.

Off the top of my head, I detect a top-right Mongolian-Manchu-Tibetan quadrant (note that Mongolians and Tibetans are also linked by the rare haplogroup D) and a left Central/Southern Chinese ethnic quadrant. Notice the closeness of Hani to Yi, which may validate the former's oral traditions.

Finally, getting back to the controversial issue of Y-chromosome age estimation, here are the dates proposed by the authors for the age of STR variation within haplogroups and their divergence times. In my opinion these are overestimates due to the use of the evolutionary rate.

A case in point is haplogroup C3b-P39; according to the authors' date, this ought to be related to the early arrival of the ancestors of Amerindians, but haplogroup C in the Americans has a strong relationship with Na-Dene speakers such as Athapaskans, and it seems to me that a late spread of this haplogroup is more consistent with its limited geographical distribution and strong linguistic associations.

Related: the Southern origin of O3

Journal of Human Genetics doi: 10.1038/jhg.2010.40

Global distribution of Y-chromosome haplogroup C reveals the prehistoric migration routes of African exodus and early settlement in East Asia

Hua Zhong et al.

The regional distribution of an ancient Y-chromosome haplogroup C-M130 (Hg C) in Asia provides an ideal tool of dissecting prehistoric migration events. We identified 465 Hg C individuals out of 4284 males from 140 East and Southeast Asian populations. We genotyped these Hg C individuals using 12 Y-chromosome biallelic markers and 8 commonly used Y-short tandem repeats (Y-STRs), and performed phylogeographic analysis in combination with the published data. The results show that most of the Hg C subhaplogroups have distinct geographical distribution and have undergone long-time isolation, although Hg C individuals are distributed widely across Eurasia. Furthermore, a general south-to-north and east-to-west cline of Y-STR diversity is observed with the highest diversity in Southeast Asia. The phylogeographic distribution pattern of Hg C supports a single coastal ‘Out-of-Africa’ route by way of the Indian subcontinent, which eventually led to the early settlement of modern humans in mainland Southeast Asia. The northward expansion of Hg C in East Asia started ~40 thousand of years ago (KYA) along the coastline of mainland China and reached Siberia ~15 KYA and finally made its way to the Americas.

Link

Genetic methods applied to linguistic diversity of the Sahul

It is great to see cross-pollination between the sciences; in this case, use of STRUCTURE has led to insights about languages of the Sahul.

From the paper:

Although we cannot specify how many different migrations have colonized Sahul since the first settlement approximately 50,000 years ago, our results indicate ancient splits into seven major plausible groups: TNG, South-Papuan, North-West Papuan, North-East Papuan, West-Papuan, PN, and non-PN. The wide-spread families (TNG and PN) on both sides of the Torres Strait divide (~9,000 BP) are the result of more recent expansions of two of those groups, in the case of TNG probably linked to the development of agriculture, ~9,000 to 6,000 years ago, see [35],[37].

The AN expansion is much more recent and has only had effects in eastern Indonesia, along the north coast of New Guinea and the islands east of the New Guinea mainland. We know on the basis of the comparative method correlated with archaeological data that approximately 3,200 years ago the Oceanic subgroup dispersed from its homeland on New Britain in three directions [9]: (1) back along the north coast, (2) around the eastern tip of New Guinea along the south coast, and (3) much further into the Pacific. The results of our analysis capture some of the impact of this great expansion on the languages that were already in the region. We find that in the eastern islands there are clearly distinct AN and non-AN groups, with good evidence of a deep structural phylogenetic signal, albeit with some admixture [16]. In the western islands however there is considerably more typological convergence between AN and non-AN languages (see also [38]). The linguistic population identified as Red appears to have members along the north coast (Mairasi, I'saka, and Kamasau) and on New Britain, where again both AN (Mangseng) and Papuan languages (Kol and Sulka) have contributions from the same cluster. This finding suggests an area of millennia of contact between AN and Papuan non-TNG speaking groups.

Gene Expression has more.

PLoS Biology doi:10.1371/journal.pbio.1000241

Explaining the Linguistic Diversity of Sahul Using Population Models


Ger Reesink et al.

Abstract

The region of the ancient Sahul continent (present day Australia and New Guinea, and surrounding islands) is home to extreme linguistic diversity. Even apart from the huge Austronesian language family, which spread into the area after the breakup of the Sahul continent in the Holocene, there are hundreds of languages from many apparently unrelated families. On each of the subcontinents, the generally accepted classification recognizes one large, widespread family and a number of unrelatable smaller families. If these language families are related to each other, it is at a depth which is inaccessible to standard linguistic methods. We have inferred the history of structural characteristics of these languages under an admixture model, using a Bayesian algorithm originally developed to discover populations on the basis of recombining genetic markers. This analysis identifies 10 ancestral language populations, some of which can be identified with clearly defined phylogenetic groups. The results also show traces of early dispersals, including hints at ancient connections between Australian languages and some Papuan groups (long hypothesized, never before demonstrated). Systematic language contact effects between members of big phylogenetic groups are also detected, which can in some cases be identified with a diffusional or substrate signal. Most interestingly, however, there remains striking evidence of a phylogenetic signal, with many languages showing negligible amounts of admixture.

Link

Common variant for straight hair in Europeans

American Journal of Human Genetics doi:10.1016/j.ajhg.2009.10.009

Common Variants in the Trichohyalin Gene Are Associated with Straight Hair in Europeans

Sarah E. Medland et al.

Abstract

Hair morphology is highly differentiated between populations and among people of European ancestry. Whereas hair morphology in East Asian populations has been studied extensively, relatively little is known about the genetics of this trait in Europeans. We performed a genome-wide association scan for hair morphology (straight, wavy, curly) in three Australian samples of European descent. All three samples showed evidence of association implicating the Trichohyalin gene (TCHH), which is expressed in the developing inner root sheath of the hair follicle, and explaining ∼6% of variance (p = 1.5 × 10⁻³¹). These variants are at their highest frequency in Northern Europeans, paralleling the distribution of the straight-hair EDAR variant in Asian populations.

Link

Ancestry informative marker set for determining continental origin (Nassir et al. 2009)

UPDATE: This PCA plot from the paper is very instructive:




In PC1 vs PC2 (top left), the five major races (Caucasoids, East Asian Mongoloids, Amerindians, Australoids, Negroids) are clearly separable, but their relationships are not very clear. Australoids are somewhere between Caucasoids and East Asians. If we were to go by this figure alone, we might even infer that they are some type of mix of the two. But, look at PC3 vs PC4 (top right). Here it is the case that Australoids are not intermediate between Caucasoids and Mongoloids, but occupy their own space, and we can conclude that they are not in fact such a mix.

Compare with Mexicans (bottom left), who occupy the same space as East Asians in PC1 vs PC2. Does that mean that they are East Asians? An alternative explanation is that they are a mix of Caucasoids and Amerindians, since they occupy an intermediate position between the two groups, which happens to coincide with the position of East Asians. But, if we look at PC3 vs P4 (bottom right), it is clear that Mexicans are indeed better explained as a Caucasoid-Amerindian mix, as they occupy an intermediate position between Caucasoids and Columbians/Quechuans (who are on the left), and not at all that of East Asians (who are on the right).

Next, consider African Americans. In PC1 vs PC2 they occupy an intermediate position between Negroids and Caucasoids (bottom left), as expected by their known ancestry. But, what if we didn't know about their history, and we wanted to infer their origin based on their genomes, as we did with Australoids? Unlike Australoids, in PC3 vs PC4, African Americans do not form a cluster of their own, but overlap with both Caucasoids and Negroids who occupy the same space in these two dimensions. Thus, we are more certain that they are indeed a Caucasoid-Negroid mixed population.

Next, consider Mozabites and South Asians, both of which deviate from Caucasoids, in a Negroid, and Mongoloid direction respectively (top left). North African Mozabites may indeed by Negroid-influenced, as is evident in the STRUCTURE analysis of this paper. South Asian Indians, however, who show "admixture" with the East Asian cluster at K=5 in the STRUCTURE analysis, are revealed to form a cluster of their own at higher K (pink), suggesting that they are not, in fact a Caucasoid-Mongoloid mixed population.

The important lesson from all of this, is to use as much information as possible when trying to examine population relationships from graphical plots, because things may not always be "what they seem", and a number of alternative explanations may result in identical two-dimensional plots.

BMC Genetics 2009, 10:39doi:10.1186/1471-2156-10-39

An ancestry informative marker set for determining continental origin: validation and extension using human genome diversity panels

Rami Nassir et al.

Abstract (provisional)

Background

Case-control genetic studies of complex human diseases can be confounded by population stratification. This issue can be addressed using panels of ancestry informative markers (AIMs) that can provide substantial population substructure information. Previously, we described a panel of 128 SNP AIMs that were designed as a tool for ascertaining the origins of subjects from Europe, Sub-Saharan Africa, Americas, and East Asia.

Results

In this study, genotypes from Human Genome Diversity Panel populations were used to further evaluate a 93 SNP AIM panel, a subset of the 128 AIMS set, for distinguishing continental origins. Using both model-based and relatively model-independent methods, we here confirm the ability of this AIM set to distinguish diverse population groups that were not previously evaluated. This study included multiple population groups from Oceana, South Asia, East Asia, Sub-Saharan Africa, North and South America, and Europe. In addition, the 93 AIM set provides population substructure information that can, for example, distinguish Arab and Ashkenazi from Northern European population groups and Pygmy from other Sub-Saharan African population groups.

Conclusion

These data provide additional support for using the 93 AIM set to efficiently identify continental subject groups for genetic studies, to identify study population outliers, and to control for admixture in association studies.

Link

The missing mtDNA link in the southern route out of Africa

In order to substantiate the southern route hypothesis of the settlement of Australia, a link between Australia and coastal populations of Asia is needed. Australian mtDNA belongs largely to the same Out-of-Africa subclades M and N, but it is not clearly a branch of a more derived clade that would allow us to pinpoint a specific Eurasian location as a place of origin.

This paper makes the case that Australian mtDNA haplogroup M42 shares two polymorphisms with a set of Indian M sequences, suggesting more recent common ancestry between these Indians and Australians than the generic "Out of Africa" M. The simplest explanation for this is that the M42 ancestors of Australians ultimately originated in India, and were thus part of the "southern route" dispersal of humans from Africa.

BMC Evolutionary Biology 2009, 9:173doi:10.1186/1471-2148-9-173

Reconstructing Indian-Australian phylogenetic link.

Satish Kumar et al.

Abstract

Background
An early dispersal of biologically and behaviorally modern humans from their African origins to Australia, by at least 45 thousand years via southern Asia has been suggested by studies based on morphology, archaeology and genetics. However, mtDNA lineages sampled so far from south Asia, eastern Asia and Australasia show non-overlapping distributions of haplogroups within pan Eurasian M and N macrohaplogroups. Likewise, support from the archaeology is still ambiguous.

Results
In our completely sequenced 966-mitochondrial genomes from 26 relic tribes of India, we have identified seven genomes, which share two synonymous polymorphisms with the M42 haplogroup, which is specific to Australian Aborigines.

Conclusions
Our results showing a shared mtDNA lineage between Indians and Australian Aborigines provides direct genetic evidence of an early colonization of Australia through south Asia, following the "southern route".

Link

Relationship of cranial robusticity to cranial form, geography and climate

UPDATE (June 30)
This paper investigates the relationship between cranial robusticity and a number of factors said to underlie it, including cranial size and shape, climate, and neutral genetic variation. Genetic similarity between populations was assessed using the well-known Rosenberg et al. dataset from 2002.

From the paper:

If the robusticity traits are the subject of neutral evolutionary processes, then the distance matrix based on these characters will be strongly correlated with that based on the neutral genetic markers (microsatellite data) (e.g., Roseman, 2004).

...

A functional hypothesis that specifically implicates forces associated with mastication would be supported by a stronger correlation between cranial robusticity and the MLS rather than CLS as the former more directly captures morphology associated with mastication, although it is also possible that changes in overall
cranial shape may be related to mastication. A strong relationship between cranial robusticity and the climatic variables would support the influence of the local environment on the development of cranial robusticity.

Note: CLS/MLS=cranial/masticatory landmark set.

First of all, it turns out that Robusticity traits are closely correlated with each other, suggesting that they do indeed capture an overall factor of "Robusticity" rather than being independent from each other. A notable exception is occipital torus, which is not significantly related to other robusticity traits.

Next up, principal components analysis was performed:

In deciding how many PCs to evaluate, we applied the common Guttman-Kaiser criterion (keep all PCs with eigenvalues [1.0; Kaiser, 1961), which results in the retention of the first three components. However, a more conservative criterion, the Scree Plot (Cattell, 1966), suggests that only PC 1 should be retained. Although PC 1 accounted for a proportionally larger percentage of the total variance in cranial robusticity (27%), the second and third components each explain 11% of the variance and may indicate that there is more than one relevantpattern of cranial robusticity (Table 10).

...

The first PC reflects overall levels of robusticity as all 11 traits load positively (Table 10), although the occipital torus has a loading near zero. ... The groups with the highest median (and mean) scores are New Zealand, Australia/Tasmania, North
America, and South America, while the lowest scores belong to Mongolia, East Asia, Inuit, and Khoe-San (see Fig. 3).

...

Males score significantly higher than females on PC 1 within all groups except the East and West Europeans, East and West Africans, and Khoe-San (Table 11), but males scored higher on average than females even in those groups that did not reach statistical significance

Interestingly, in the test for sex differences in PC1, Europeans differed from each other. Southern Europeans (Peloponnesian Greeks and Italians) were most dimorphic, and West Europeans (Austrians and Germans) were least.

From the paper:

The second PC has both high positive (occipital torus, rounding of orbits) and high negative (sagittal keel, anterior mastoid, bregmatic eminence) loadings ... The highest scoring groups on PC 2 are East Asia, Mongolia, Australia/Tasmania, and the Khoe-San, while East Africa, West Africa, and Eastern Europe have low scores (Fig. 3a). Many of the pair-wise contrasts between the highest and lowest scoring groups are significant, particularly those that include East Africa, East Asia, and Mongolia (Table 10). It appears that while the East Asian populations are gracile overall (see above), they do display some characters typically considered as ‘‘robust’’ (e.g., the occipital torus).

...

The third PC also has a mixed pattern of positive and negative loadings. The traits with the highest loadings are sagittal keel, occipital torus, malar tubercle, bregmatic
eminence (all positive), infraglabellar notch and supraorbital torus (both negative). The North American and, to a lesser extent, New Zealand, groups score highest
on PC 3, in contrast to Australia/Tasmania, Southern Europe, Eastern Europe, and East Africa (Fig. 3b).

In PC1, sex and size differences contribute about 36% of the variation, but only 3 and 8% in PC2 an PC3 respectively.

The author calculated distances between populations for Robusticity, CLS, MLS, Climate, and microsatellites, and sees how the inter-population distance based on robusticity correlates with the other four potentially explanatory factors:

The correlation coefficients from the Mantel tests are weak, ranging from -0.115 to 0.387 (Table 12). The null hypothesis of neutral evolution was rejected as the robusticity distances were not significantly correlated with neutral genetic distances.

The strongest (and only significant) correlations are between cranial robusticity and cranial (CLS) or masticatory apparatus shape (MLS). Cranial robusticity in the combined male–female sample is significantly correlated with the masticatory shape, and its correlation with overall cranial shape approached significance (Table 12).

On the Southern European masticatory system:

Whereas South Europe is among the lowest scoring groups on both the shape and robusticity vectors, the highest scoring groups on the robusticity vector (e.g., South America and New Zealand) are not the highest scoring groups on the shape vector (specifically Australia/Tasmania). The more gracile groups (e.g., South European) have more anteriorly positioned zygomatic bones (as indicated by the inferior zygomaticotemporal suture and zygomaxillare), more laterally located postglenoid processes and frontotemporale, and relatively larger cheek teeth (in the anteroposterior direction) that are more superiorly positioned.

Finally, a bit on Australian aboriginals who often get singled out as being particularly robust. It turns out that they are, but their pattern of robusticity involves particular traits, while other human groups, such as Native Americans are robust in a different manner:

While Aboriginal Australians have long been the standard bearers for robust cranial morphology, this study reveals that human populations exhibit more than one pattern of cranial robusticity. The results of this study emphasize a primary trend of variability from gracile to robust (except in the occipital torus region), but also highlight secondary patterns of differential cranial trait expression within populations. For example, the Native American group from Grand Gulch, Utah is characterized by robust expression of the sagittal keel, bregmatic eminence, occipital torus, and malar tubercle, but a more gracile supraorbital region in contrast to the pattern seen in Aboriginal Australians.

All in all, this is an excellent data-driven paper, which combines data from skulls, genes, and climate to arrive at a comprehensive study of the phenomenon of modern human cranial robusticity and its etiology.


American Journal of Physical Anthropology doi:10.1002/ajpa.21120

Relationship of cranial robusticity to cranial form, geography and climate in Homo sapiens

Karen L. Baab et al.

Abstract

Variation in cranial robusticity among modern human populations is widely acknowledged but not well-understood. While the use of robust cranial traits in hominin systematics and phylogeny suggests that these characters are strongly heritable, this hypothesis has not been tested. Alternatively, cranial robusticity may be a response to differences in diet/mastication or it may be an adaptation to cold, harsh environments. This study quantifies the distribution of cranial robusticity in 14 geographically widespread human populations, and correlates this variation with climatic variables, neutral genetic distances, cranial size, and cranial shape. With the exception of the occipital torus region, all traits were positively correlated with each other, suggesting that they should not be treated as individual characters. While males are more robust than females within each of the populations, among the independent variables (cranial shape, size, climate, and neutral genetic distances), only shape is significantly correlated with inter-population differences in robusticity. Two-block partial least-squares analysis was used to explore the relationship between cranial shape (captured by three-dimensional landmark data) and robusticity across individuals. Weak support was found for the hypothesis that robusticity was related to mastication as the shape associated with greater robusticity was similar to that described for groups that ate harder-to-process diets. Specifically, crania with more prognathic faces, expanded glabellar and occipital regions, and (slightly) longer skulls were more robust than those with rounder vaults and more orthognathic faces. However, groups with more mechanically demanding diets (hunter-gatherers) were not always more robust than groups practicing some form of agriculture.

Link