Sima de los Huesos hominins were Proto-Neandertals

Nature (2016) doi:10.1038/nature17405

Nuclear DNA sequences from the Middle Pleistocene Sima de los Huesos hominins

Matthias Meyer, Juan-Luis Arsuaga, Cesare de Filippo, Sarah Nagel, Ayinuer Aximu-Petri, Birgit Nickel, Ignacio Martínez, Ana Gracia, José María Bermúdez de Castro, Eudald Carbonell, Bence Viola, Janet Kelso, Kay Prüfer & Svante Pääbo

A unique assemblage of 28 hominin individuals, found in Sima de los Huesos in the Sierra de Atapuerca in Spain, has recently been dated to approximately 430,000 years ago1. An interesting question is how these Middle Pleistocene hominins were related to those who lived in the Late Pleistocene epoch, in particular to Neanderthals in western Eurasia and to Denisovans, a sister group of Neanderthals so far known only from southern Siberia. While the Sima de los Huesos hominins share some derived morphological features with Neanderthals, the mitochondrial genome retrieved from one individual from Sima de los Huesos is more closely related to the mitochondrial DNA of Denisovans than to that of Neanderthals2. However, since the mitochondrial DNA does not reveal the full picture of relationships among populations, we have investigated DNA preservation in several individuals found at Sima de los Huesos. Here we recover nuclear DNA sequences from two specimens, which show that the Sima de los Huesos hominins were related to Neanderthals rather than to Denisovans, indicating that the population divergence between Neanderthals and Denisovans predates 430,000 years ago. A mitochondrial DNA recovered from one of the specimens shares the previously described relationship to Denisovan mitochondrial DNAs, suggesting, among other possibilities, that the mitochondrial DNA gene pool of Neanderthals turned over later in their history.

Link

Ancestors of Eastern Neandertals admixed with modern humans 100 thousand years ago

If true, this is very hard to reconcile with late (60kya) out of Africa and may be a smoking gun for pre-100kya presence of anatomically modern humans in Eurasia. From the paper:

The inferred demographic model confirms and provides quantitative estimates of previously inferred gene flow events among modern and archaic humans2, 3 (Extended Data Fig. 1). These include Neanderthal gene flow into modern humans outside Africa (3.3–5.8%) and gene flow from an unknown archaic hominin into the ancestors of Denisovans (0.0–0.5%). Interestingly, we also detect a signal of gene flow from modern humans into the ancestors of the Altai Neanderthal (1.0–7.1%). The precise source of this gene flow is unclear, but it appears to come from a population that either split from the ancestors of all present-day Africans or from one of the early African lineages, as significant admixture rates are estimated from San as well as Yoruba individuals. This introgression thus occurred in the opposite direction from the previously reported gene flow from Neanderthals to modern humans outside Africa

And:

However, it is clear that the source of the gene flow is a population equally related to present-day Africans and non-Africans (Extended Data Fig. 3). We conclude that the introgressing population diverged from other modern human populations before or shortly after the split between the ancestors of San and other Africans (Fig. 3a), which occurred approximately 200,000 years ago11.

The implications of this inference (if correct) for modern human origins are potentially monumental as they suggest a Eurasian modern human lineage (only detected in the Altai Neandertal) that diverges from other modern humans as early (if not earlier) than any two African ones.

If the new discovery checks out, it will no longer be possible to assert that the deepest split in our species, H. sapiens, involves African populations. A modest interpretation of these results would assert an earlier (pre-100kya) exodus of our species from Africa, and a more bold one would seek to re-examine the geographical origin of H. sapiens itself. I don't know if anyone is working on getting DNA from the progressive Neandertals of the Near East, but they should.

Things are bound to get more interesting.

Nature (2016) doi:10.1038/nature16544

Ancient gene flow from early modern humans into Eastern Neanderthals

Martin Kuhlwilm, Ilan Gronau, Melissa J. Hubisz, Cesare de Filippo, Javier Prado-Martinez, Martin Kircher, Qiaomei Fu, Hernán A. Burbano, Carles Lalueza-Fox, Marco de la Rasilla, Antonio Rosas, Pavao Rudan, Dejana Brajkovic, Željko Kucan, Ivan Gušic, Tomas Marques-Bonet, Aida M. Andrés, Bence Viola, Svante Pääbo, Matthias Meyer, Adam Siepel & Sergi Castellano

It has been shown that Neanderthals contributed genetically to modern humans outside Africa 47,000–65,000 years ago. Here we analyse the genomes of a Neanderthal and a Denisovan from the Altai Mountains in Siberia together with the sequences of chromosome 21 of two Neanderthals from Spain and Croatia. We find that a population that diverged early from other modern humans in Africa contributed genetically to the ancestors of Neanderthals from the Altai Mountains roughly 100,000 years ago. By contrast, we do not detect such a genetic contribution in the Denisovan or the two European Neanderthals. We conclude that in addition to later interbreeding events, the ancestors of Neanderthals from the Altai Mountains and early modern humans met and interbred, possibly in the Near East, many thousands of years earlier than previously thought.

Link

Y chromosomes and Catalan surnames

Some really rich data in the supplements.

European Journal of Human Genetics advance online publication 18 February 2015; doi: 10.1038/ejhg.2015.14

Y-chromosome diversity in Catalan surname samples: insights into surname origin and frequency

Neus Solé-Morata et al.

The biological behavior of the Y chromosome, which is paternally inherited, implies that males sharing the same surname may also share a similar Y chromosome. However, socio-cultural factors, such as polyphyletism, non-paternity, adoption, or matrilineal surname transmission, may prevent the joint transmission of the surname and the Y chromosome. By genotyping 17 Y-STRs and 68 SNPs in ~2500 male samples that each carried one of the 50 selected Catalan surnames, we could determine sets of descendants of a common ancestor, the population of origin of the common ancestor, and the date when such a common ancestor lived. Haplotype diversity was positively correlated with surname frequency, that is, rarer surnames showed the strongest signals of coancestry. Introgression rates of Y chromosomes into a surname by non-paternity, adoption, and transmission of the maternal surname were estimated at 1.5−2.6% per generation, with some local variation. Average ages for the founders of the surnames were estimated at ~500 years, suggesting a delay between the origin of surnames (twelfth and thirteenth centuries) and the systematization of their paternal transmission. We have found that, in general, a foreign etymology for a surname does not often result in a non-indigenous origin of surname founders; however, bearers of some surnames with an Arabic etymology show an excess of North African haplotypes. Finally, we estimate that surname prediction from a Y-chromosome haplotype, which may have interesting forensic applications, has a ~60% sensitivity but a 17% false discovery rate.

Link

A story of 69 ancient Europeans

A new study on the bioRxiv includes data on 69 ancient Europeans (remember when we got excited in anticipation for the single genome of the Iceman? that was only three years ago) and adds plenty of new info to chew on for those of us interested in prehistory. 

Two Near Eastern migrations into Europe

In 2011, I observed that West Eurasian populations were too close (measured by Fst) to allow for long periods of differentiation between them. By implication, there must have been a "common source" of ancestry uniting them, which I placed in a "womb of nations" of the Neolithic Near East. I proposed that migrations out of this core area homogenized West Eurasians, writing:

In Arabia, the migrants would have met aboriginal Arabians, similar to their next door-neighbors in East Africa, undergoing a subtle African shift (Southwest_Asians). In North Africa, they would have encountered denser populations during the favorable conditions of MIS 1, and by absorbing them they would became the Berbers (Northwest_Africans). Their migrations to the southeast brought them into the realm of Indian-leaning people, in the rich agricultural fields of the Mehrgarh and the now deserted oases of Bactria and Margiana. Across the Mediterranean and along the Atlantic facade of Europe, they would have encountered the Mesolithic populations of Europe, and through their blending became the early Neolithic inhabitants of the Mediterranean and Atlantic coasts of Europe (Mediterraneans). And, to the north, from either the Balkans, the Caucasus, or the trans-Caspian region, they would have met the last remaining Proto-Europeoid hunters of the continental zone, becoming the Northern Europeoids who once stretched all the way to the interior of Asia.

The new paper confirms the last two of these migrations. The remainder involve parts of the world from which no ancient DNA has been studied.

The first migration (early Neolithic) is already uncontroversial, but the paper includes data from Spanish early farmers that are also Sardinian- and LBK-like. The "Sardinian" Iceman was no fluke. It is now proven that not only the LBK but also the Spanish Neolithic came from the same expansion of Mediterranean populations which survives in Sardinia. The authors write:

Principal components analysis (PCA) of all ancient individuals along with 777 present-day West Eurasians4 (Fig. 2a, SI5) replicates the positioning of present-day Europeans between the Near East and European hunter-gatherers4,20, and the clustering of early farmers from across Europe with present day Sardinians3,4,27, suggesting that farming expansions across the Mediterranean to Spain and via the Danubian route to Hungary and Germany descended from a common stock.

The second migration went into eastern Europe:

The Yamnaya differ from the EHG by sharing fewer alleles with MA1 (|Z|=6.7) suggesting a dilution of ANE ancestry between 5,000-3,000 BCE on the European steppe. This was likely due to admixture of EHG with a population related to present-day Near Easterners, as the most negative f3-statistic in the Yamnaya (giving unambiguous evidence of admixture) is observed when we model them as a mixture of EHG and present-day Near Eastern populations like Armenians (Z = -6.3; SI7).

The EHG (Eastern European Hunter-Gatherers) are likely Proto-Europeoid foragers and the Yamnaya (a Bronze Age Kurgan culture) were a mixture of the EHG and something akin to Armenians.The "attraction" of later groups to the Near East is clear in the PCA: hunter-gatherers on the left side, the Near East (as grey dots) on the right side, and Neolithic/Bronze Age/modern Europeans in the middle. The second migration may very well be related to the Uruk expansion and the presence of gracile Mediterranoids and robust Proto-Europeoids in the Yamna:

The Yamna population generally belongs to the European race. It was tall (175.5cm), dolichocephalic, with broad faces of medium height. Among them there were, however, more robust elements with high and wide faces of the proto-Europoid type, and also more gracile individuals with narrow and high faces, probably reflecting contacts with the East Mediterranean type (Kurts 1984: 90).

The authors present a table of Fst values which confirms the homogenizing influence of migrations from the Near East. The WHG group has an Fst=0.086 with Armenians, but the LBK farmers have only 0.023. The EHG group has an Fst=0.067 with Armenians, but the Yamnaya steppe people have only 0.030. Someone might argue that it is the Armenians that are receiving genes from Europe, but the same pattern holds even for the Bedouins, for which admixture with Europeans seems far-fetched: 0.106 to 0.043 and 0.093 to 0.060. It is now clear that the "glue" that did not allow West Eurasian populations to drift very far apart were migrations from the Near East.

The (partial) demise of the farmers

It seems that the legacy of the early farmers suffered two hits, which is why only in Sardinia and (to a lesser degree) in southern Europe that they have persisted as the major component of ancestry. The first blow came during the Neolithic:

Middle Neolithic Europeans from Germany, Spain, Hungary, and Sweden from the period ~4,000-3,000 BCE are intermediate between the earlier farmers and the WHG, suggesting an increase of WHG ancestry throughout much of Europe.

And the coup de grâce after the 5kya mark:

We estimate that these two elements each contributed about half the ancestry each of the Yamnaya (SI6, SI9), explaining why the population turnover inferred using Yamnaya as a source is about twice as high compared to the undiluted EHG. The estimate of Yamnaya related ancestry in the Corded Ware is consistent when using either present populations or ancient Europeans as outgroups (SI9, SI10), and is 73.1 ± 2.2% when both sets are combined (SI10). [...] The magnitude of the population turnover that occurred becomes even more evident if one considers the fact that the steppe migrants may well have mixed with eastern European agriculturalists on their way to central Europe. Thus, we cannot exclude a scenario in which the Corded Ware arriving in today’s Germany had no ancestry at all from local populations.

Confirmation of the Bronze Age Indo-European invasion of Europe

In 2012 I had used the paltry data on a handful ancient DNA samples to observe that in ADMIXTURE modern Europeans had a West Asian genetic component (peaking in "Caucasus" and "Gedrosia") that pre-5kya Europeans didn't. I proposed that the Bronze Age migration of the Indo-Europeans spread this component:

But there is another component present in modern Europe, the West_Asian which is conspicuous in its absence in all the ancient samples so far. This component reaches its highest occurrence in the highlands of West Asia, from Anatolia and the Caucasus all the way to the Indian subcontinent. [...] Nonetheless, some of the legacy of the earliest Indo-European speakers does appear to persist down to the present day in the genomes of their linguistic descendants, and I predict that when we sample later (post 5-4kya) individuals we will finally find the West_Asian piece that is missing from the European puzzle.

This prediction is now confirmed:

This pattern is also seen in ADMIXTURE analysis (Fig. 2b, SI6), which implies that the Yamnaya have ancestry from populations related to the Caucasus and South Asia that is largely absent in 38 Early or Middle Neolithic farmers but present in all 25 Late Neolithic or Bronze Age individuals. This ancestry appears in Central Europe for the first time in our series with the Corded Ware around 2,500 BCE (SI6, Fig. 2b, Extended Data Fig. 1).

I was a little puzzled with the "Ancient North Eurasians" recently proposed as a "third ancestral population" for Europeans: it seemed to be a tertium quid that spread after 5kya, but very different geographically than the "West Asian" component. But:

These results can be explained if the new genetic material that arrived in Germany was a composite of two elements: EHG and a type of Near Eastern ancestry different from that which was introduced by early farmers (also suggested by PCA and ADMIXTURE; Fig. 2, SI5, SI6).

So, it seems that there is no contradiction after all and both EHG (which is related to "Ancient North Eurasians") and another type of Near Eastern ancestry (=West_Asian) arrived after 5kya.

1939 strikes back

It is amazing how well this was anticipated by Carleton Coon in 1939. Back then much of West Eurasia was an archaeological/anthropological terra incognita, there was no radiocarbon dating, no DNA, no computers, not even serious multivariate statistics. And yet:

We shall see, in our survey of prehistoric European racial movements, 8 that the Danubian agriculturalists of the Early Neolithic brought a food-producing economy into central Europe from the East. They perpetuated in the new European setting a physical type which was later supplanted in their original home. Several centuries later the Corded people, in the same way, came from southern Russia but there we first find them intermingled with other peoples, and the cul-tural factors which we think of as distinctively Corded are included in a larger cultural equipment. [...] On the basis of the physical evidence as well, it is likely that the Corded people came from somewhere north or east of the Black Sea. The fully Neolithic crania from southern Russia which we have just studied include such a type, also seen in the midst of Sergi's Kurgan aggregation. Until better evidence is produced from elsewhere, we are entitled to consider southern Russia the most likely way station from which the Corded people moved westward.

And in 2015:

Our results support a view of European pre-history punctuated by two major migrations: first, the arrival of first farmers during the Early Neolithic from the Near East, and second of Yamnaya pastoralists during the Late Neolithic from the steppe (Extended Data Fig. 5).

In 1939:

Linguistically, Indo-European is probably a relatively recent phenomenon, which arose after animals had been tamed and plants cultivated. The latest researches find it to be a derivative of an initially mixed language, whose principal elements were Uralic, called element A, and some undesignated element B which was probably one of the eastern Mediterranean or Caucasic languages. 5 The plants and animals on which the Somewhere in the plains of southern Russia or central Asia, the blending of languages took place which resulted in Indo-European speech. This product in turn spread and split, and was further differentiated by mixture with the languages of peoples upon whom it, in one form or other, was imposed. Some of the present Indo-European languages, in addition to these later accretions from non-Indo-European tongues, contain more of the A element than others, which contain more of the B. The unity of the original " Indo- Europeans," could not have been of long duration, if it was ever complete. 

In 2015:

These results can be explained if the new genetic material that arrived in Germany was a composite of two elements: EHG and a type of Near Eastern ancestry different from that which was introduced by early farmers (also suggested by PCA and ADMIXTURE; Fig. 2, SI5, SI6). We estimate that these two elements each contributed about half the ancestry each of the Yamnaya (SI6, SI9), explaining why the population turnover inferred using Yamnaya as a source is about twice as high compared to the undiluted EHG.

The EHG is still flimsy as it's only two individuals from Karelia and Samara who are very similar to each other. It's hard not to imagine that the hunter-gatherer from Russian Karelia (outside any proposed PIE homeland) would be speaking a similar language as his Samara counterpart. Did they both speak "element A" and was PIE formed when the "southern" steppe hunter-gatherers came into contact with "element B" people from the Caucasus? Short of a time machine, we can never say for sure. This might very well be an answer to the conundrum of Uralic/Proto-Kartvelian borrowings. There is simply no geographical locale in which these two language families neighbor each other: Northwest, Northeast Caucasian speakers and the pesky Greater Caucasus intervene. But, maybe there was no such locale, and these borrowings aren't due to some "PIE people" living adjacent to Uralic and Proto-Karvelian speakers but the "PIE people" being a mix of an element A (EHG) that was (or interacted with) Uralic and another element B (Armenian-like) that was (or interacted with) Proto-Kartvelian.

Urheimat (or not?)

The authors of the current paper are agnostic about the PIE homeland:

We caution that the location of the Proto-Indo-European9,27,29,30 homeland that also gave rise to the Indo-European languages of Asia, as well as the Indo-European languages of southeastern Europe, cannot be determined from the data reported here (SI11). Studying the mixture in the Yamnaya themselves, and understanding the genetic relationships among a broader set of ancient and present-day Indo-European speakers, may lead to new  insight about the shared homeland.

Whatever the ultimate answer will be, it seems that Coon was right that "The unity of the original " Indo- Europeans," could not have been of long duration, if it was ever complete." If PIE=EHG (as Anthony and Ringe suggest), then "from the crib", PIE got half its ancestry from a non-IE, Near Eastern source. Conversely, if PIE=Near East (as I suggested) then "from the crib", PIE got half of its ancestry from a non-IE, Eastern European source. The "Yamnaya" seems to max out in Norwegians at around half, which means that they are about a quarter Proto-Indo-European genetically, regardless of which theory is right.

These two possibilities (as well as the third one of PIE being neither-nor, but rather a linguistic mixture of the languages of the EHG and Near East) are testable. The Anthony/Ringe version of the steppe hypothesis predicts pre-Yamnaya expansions from the steppe. Whether these happened and what was their makeup can be tested: if they did occur and they did lack "Near Eastern" ancestry, then the steppe hypothesis will be proven. PIE in the Near East, on the other hand, predicts that some PIE languages (certainly the Anatolian ones) will be a "within the Near East" expansion. If such migrations did occur and they lacked "EHG" ancestry, then some variant of the Gamkrelidze/Ivanov model will be proven. Or, the truth might be that everywhere where Indo-Europeans arrive they carry a blend of "West Asian" and "EHG", supporting the third possibility. Time will tell.

In the interim, I am curious about how much Yamnaya ancestry existed in different parts of Europe (all of the post-5kya samples in this study come from Germany, with a couple from Hungary). In northern Europe, all populations seem to have less Yamnaya ancestry than the Corded Ware: there it must have declined. But, modern Hungarians have more than Bronze Age Hungarians: there it must have increased.

Germany and a slice of Hungary is a very narrow window through which to see the whole of Europe and these results must be tested by looking at samples from beyond the "heartland". I do hope that some kind of Moore's law operates in the world of ancient DNA, and in three more years we'll be reading studies about thousands of ancient individuals.

bioRxiv doi: http://dx.doi.org/10.1101/013433
Massive migration from the steppe is a source for Indo-European languages in Europe

Wolfgang Haak , Iosif Lazaridis , Nick Patterson , Nadin Rohland , Swapan Mallick , Bastien Llamas , GuidoBrandt , Susanne Nordenfelt , Eadaoin Harney , Kristin Stewardson , Qiaomei Fu , Alissa Mittnik , Eszter Banffy ,Christos Economou , Michael Francken , Susanne Friederich , Rafael Garrido Pena , Fredrik Hallgren , ValeryKhartanovich , Aleksandr Khokhlov , Michael Kunst , Pavel Kuznetsov , Harald Meller , Oleg Mochalov ,Vayacheslav Moiseyev , Nicole Nicklisch , Sandra L. Pichler , Roberto Risch , Manuel A. Rojo Guerra , ChristinaRoth , Anna Szecsenyi-Nagy , Joachim Wahl , Matthias Meyer , Johannes Krause , Dorcas Brown , DavidAnthony , Alan Cooper , Kurt Werner Alt , David Reich

We generated genome-wide data from 69 Europeans who lived between 8,000-3,000 years ago by enriching ancient DNA libraries for a target set of almost four hundred thousand polymorphisms. Enrichment of these positions decreases the sequencing required for genome-wide ancient DNA analysis by a median of around 250-fold, allowing us to study an order of magnitude more individuals than previous studies and to obtain new insights about the past. We show that the populations of western and far eastern Europe followed opposite trajectories between 8,000-5,000 years ago. At the beginning of the Neolithic period in Europe, ~8,000-7,000 years ago, closely related groups of early farmers appeared in Germany, Hungary, and Spain, different from indigenous hunter-gatherers, whereas Russia was inhabited by a distinctive population of hunter-gatherers with high affinity to a ~24,000 year old Siberian6. By ~6,000-5,000 years ago, a resurgence of hunter-gatherer ancestry had occurred throughout much of Europe, but in Russia, the Yamnaya steppe herders of this time were descended not only from the preceding eastern European hunter-gatherers, but from a population of Near Eastern ancestry. Western and Eastern Europe came into contact ~4,500 years ago, as the Late Neolithic Corded Ware people from Germany traced ~3/4 of their ancestry to the Yamnaya, documenting a massive migration into the heartland of Europe from its eastern periphery. This steppe ancestry persisted in all sampled central Europeans until at least ~3,000 years ago, and is ubiquitous in present-day Europeans. These results provide support for the theory of a steppe origin of at least some of the Indo-European languages of Europe.

Link

mtDNA from Chalcolithic Iberia (El Mirador cave)

A very exciting new study from Chalcolithic Iberia. The authors compare their mtDNA data with those from the Brandt et al. (2013) paper which includes German samples from the same time.

The following plot seems quite useful. From its caption:

This study: El Mirador (MIR). Published prehistoric cultures [21]: Hunter-gatherer central (HGC), Linear Pottery culture (LBK), Rössen culture (RSC), Schöningen group (SCG), Baalberge culture (BAC), Salzmünde culture (SMC), Bernburg culture (BEC), Corded Ware culture (CWC), Bell Beaker culture (BBC), Unetice culture (UC), Funnel Beaker culture (FBC), Pitted Ware culture (PWC), Hunter-Gatherer south (HGS), (Epi) Cardial (CAR), Neolithic Portugal (NPO), Neolithic Basque Country and Navarre (NBQ), Treilles culture (TRE), Hunter-gatherer east (HGE), Bronze Age Siberia (BAS), Bronze Age Kazakhstan (BAK).

From the paper:

In none of the analyses El Mirador sample shows close genetic affinities with a contemporaneous Bell Beaker population of 29 specimens gathered from three sites in Germany. The Bell Beaker mtDNA signal is characterized by high frequencies (around 50%) of H haplogroup that in El Mirador only reaches 26%. This heterogeneity in the genetic composition of geographically close populations adds further complexity to future reconstructions of these ancient expansions and correlates with the existence of contemporaneous groups with and without the typical Bell Beaker burial kit.

mtDNA may not be the best tool for studying the spread of Bell Beakers (if this involved men), but this shows that the high frequency of H in Bell Beakers of Germany (observed by Brandt et al.) is not due to an even higher frequency of H in Iberia.

PLoS ONE 9(8): e105105. doi:10.1371/journal.pone.0105105

Mitochondrial DNA from El Mirador Cave (Atapuerca, Spain) Reveals the Heterogeneity of Chalcolithic Populations

Daniel Gómez-Sánchez,Iñigo Olalde et al.

Previous mitochondrial DNA analyses on ancient European remains have suggested that the current distribution of haplogroup H was modeled by the expansion of the Bell Beaker culture (ca 4,500–4,050 years BP) out of Iberia during the Chalcolithic period. However, little is known on the genetic composition of contemporaneous Iberian populations that do not carry the archaeological tool kit defining this culture. Here we have retrieved mitochondrial DNA (mtDNA) sequences from 19 individuals from a Chalcolithic sample from El Mirador cave in Spain, dated to 4,760–4,200 years BP and we have analyzed the haplogroup composition in the context of modern and ancient populations. Regarding extant African, Asian and European populations, El Mirador shows affinities with Near Eastern groups. In different analyses with other ancient samples, El Mirador clusters with Middle and Late Neolithic populations from Germany, belonging to the Rössen, the Salzmünde and the Baalberge archaeological cultures but not with contemporaneous Bell Beakers. Our analyses support the existence of a common genetic signal between Western and Central Europe during the Middle and Late Neolithic and points to a heterogeneous genetic landscape among Chalcolithic groups.

Link

Early Neandertal disappearance in Iberia

Journal of Human Evolution DOI: 10.1016/j.jhevol.2014.06.002

New evidence of early Neanderthal disappearance in the Iberian Peninsula

Bertila Galván et al.

The timing of the end of the Middle Palaeolithic and the disappearance of Neanderthals continue to be strongly debated. Current chronometric evidence from different European sites pushes the end of the Middle Palaeolithic throughout the continent back to around 42 thousand years ago (ka). This has called into question some of the dates from the Iberian Peninsula, previously considered as one of the last refuge zones of the Neanderthals. Evidence of Neanderthal occupation in Iberia after 42 ka is now very scarce and open to debate on chronological and technological grounds. Here we report thermoluminescence (TL) and optically stimulated luminescence (OSL) dates from El Salt, a Middle Palaeolithic site in Alicante, Spain, the archaeological sequence of which shows a transition from recurrent to sporadic human occupation culminating in the abandonment of the site. The new dates place this sequence within MIS 3, between ca. 60 and 45 ka. An abrupt sedimentary change towards the top of the sequence suggests a strong aridification episode coinciding with the last Neanderthal occupation of the site. These results are in agreement with current chronometric data from other sites in the Iberian Peninsula and point towards possible breakdown and disappearance of the Neanderthal local population around the time of the Heinrich 5 event. Iberian sites with recent dates (less than 40 ka) attributed to the Middle Palaeolithic should be revised in the light of these data.

Link

Sima de los Huesos hominins: ~430 thousand years old and on the Neandertal lineage

Science 20 June 2014: Vol. 344 no. 6190 pp. 1358-1363 DOI: 10.1126/science.1253958

Neandertal roots: Cranial and chronological evidence from Sima de los Huesos

J. L. Arsuaga et al.

Seventeen Middle Pleistocene crania from the Sima de los Huesos site (Atapuerca, Spain) are analyzed, including seven new specimens. This sample makes it possible to thoroughly characterize a Middle Pleistocene hominin paleodeme and to address hypotheses about the origin and evolution of the Neandertals. Using a variety of techniques, the hominin-bearing layer could be reassigned to a period around 430,000 years ago. The sample shows a consistent morphological pattern with derived Neandertal features present in the face and anterior vault, many of which are related to the masticatory apparatus. This suggests that facial modification was the first step in the evolution of the Neandertal lineage, pointing to a mosaic pattern of evolution, with different anatomical and functional modules evolving at different rates.

Link

Brown-skinned, blue-eyed, Y-haplogroup C-bearing European hunter-gatherer from Spain (Olalde et al. 2014)

There is nothing like a little ancient DNA weirdness to start off 2014, which promises to be as exciting as 2013 was.

The new study La Brana 1 identifies it as ancestral in the SLC24A5 locus in which virtually all Europeans are derived. This comes in the heels of the Loschbour preprint which identified that sample from Luxembourg as also being ancestral. Taken together, it's now clear that hunter-gatherers from Mesolithic Western Europe were brown.

Curiously, it now seems that both Europe and India were (in part) inhabited by brown people and became lighter by a process of admixture + selection. The process went "all the way" in Europe, but a cline of pigmentation was sustained in India.

The other finding (not mentioned in the abstract) is that La Brana 1 belonged to Y-haplogroup C6! This is a low-frequency European clade of haplogroup C. So now, we have evidence that haplogroup C is not eastern Eurasian (as the presence of its subclades in Australia, India, East Asia, and the Americas might suggest), but a pan-Eurasian entity. It remains to be seen whether this C-in-Europe can be pushed further back in time, but finding it in Mesolithic Iberia reduces the chance that it's some random eastern Eurasian who made it to the outskirts of Europe recently.

Finally, La Brana 1 has derived alleles at loci associated with pathogen resistance. This might be important, because a common hypothesis is that Europeans developed this type of resistance during the Neolithic as they started interacting with the pathogens of domesticated species and started living in less-hygienic higher-density settlements.


Nature (2014) doi:10.1038/nature12960

Derived immune and ancestral pigmentation alleles in a 7,000-year-old Mesolithic European

Iñigo Olalde et al.

Ancient genomic sequences have started to reveal the origin and the demographic impact of farmers from the Neolithic period spreading into Europe1, 2, 3. The adoption of farming, stock breeding and sedentary societies during the Neolithic may have resulted in adaptive changes in genes associated with immunity and diet4. However, the limited data available from earlier hunter-gatherers preclude an understanding of the selective processes associated with this crucial transition to agriculture in recent human evolution. Here we sequence an approximately 7,000-year-old Mesolithic skeleton discovered at the La Braña-Arintero site in León, Spain, to retrieve a complete pre-agricultural European human genome. Analysis of this genome in the context of other ancient samples suggests the existence of a common ancient genomic signature across western and central Eurasia from the Upper Paleolithic to the Mesolithic. The La Braña individual carries ancestral alleles in several skin pigmentation genes, suggesting that the light skin of modern Europeans was not yet ubiquitous in Mesolithic times. Moreover, we provide evidence that a significant number of derived, putatively adaptive variants associated with pathogen resistance in modern Europeans were already present in this hunter-gatherer.

Link

Lactase persistence and natural selection (Sverrisdóttir et al. 2014)

The big question is: did the present-day high allele frequency in Europeans happen because of natural selection or because of admixture with a population that was already lactase persistent?

For example, the lactase persistence allele occurs at a non-trivial frequency in present-day inhabitants of the Americas, whereas it was zero there a few thousand years ago, with the culprit being post-1492 European colonization. The frequency change in the Americas didn't happen because of natural selection, but because a new population (Europeans) moved in.

If admixture with a lactase persistent population L is at play, then the question remains how L became lactase persistent in the first place. However, this transforms the problem from (a) seeking something in the European cultural or natural environment acting as an agent of selection, into (b) seeking something in the cultural/natural environment of population L. I don't know what L might be, but seeking a population with lots of cows is a good place to start...

Mol Biol Evol (2014) doi: 10.1093/molbev/msu049

Direct estimates of natural selection in Iberia indicate calcium absorption was not the only driver of lactase persistence in Europe

Oddný Ósk Sverrisdóttir et al.

Lactase persistence (LP) is a genetically determined trait whereby the enzyme lactase is expressed throughout adult life. Lactase is necessary for the digestion of lactose – the main carbohydrate in milk – and its production is down-regulated after the weaning period in most humans and all other mammals studied. Several sources of evidence indicate that LP has evolved independently, in different parts of the world over the last 10,000 years, and has been subject to strong natural selection in dairying populations. In Europeans LP is strongly associated with, and probably caused by, a single C to T mutation 13,910bp upstream of the lactase (LCT) gene (-13,910*T). Despite a considerable body of research, the reasons why LP should provide such a strong selective advantage remains poorly understood. In this study we examine one of the most widely cited hypotheses for selection on LP – that fresh milk consumption supplements the poor vitamin D and calcium status of northern Europe's early farmers (the calcium assimilation hypothesis). We do this by testing for natural selection on -13,910*T using ancient DNA data from the skeletal remains of eight late Neolithic Iberian individuals, whom we would not expect to have poor vitamin D and calcium status because of relatively high incident UVB-light levels. None of the 8 samples successfully typed in the study had the derived T-allele. In addition, we reanalyse published data from French Neolithic remains to both test for population continuity and further examine the evolution of LP in the region. Using simulations that accommodate genetic drift, natural selection, uncertainty in calibrated radiocarbon dates, and sampling error, we find that natural selection is still required to explain the observed increase in allele frequency. We conclude that the calcium assimilation hypothesis is insufficient to explain the spread of lactase persistence in Europe.

Link

400 thousand year old human mtDNA from Sima de los Huesos

It will come to no surprise to people who noticed an earlier paper on cave bear mtDNA from Atapuerca that the folks at the Max Planck Institute would try to do the same for the plentiful human remains found in the Pit of Bones.

A new paper in Nature reports their success, and overnight increases by an order of magnitude the time depth for which we now have human mtDNA from what is commonly designated as Homo heidelbergensis, from right in the middle of the Middle Pleistocene. Obviously, this opens new vistas for archaeogenetic research, making it possible to directly look at early pre-sapiens forms of humans, and not only on their final forms prior to their replacement, the Neandertals and Denisovans.

The most impressive aspect of the new paper is most likely the technical challenges that the researchers must've overcome to achieve this result. The cave bear DNA showed that this was possible, but human DNA adds an additional complication in the form of contamination by a closely related species, us.

But, the new evolutionary result which will interest those of us not interested in the minutiae of biomolecules will no doubt be the fact that the Sima hominin's mtDNA formed a clade with the much more recent Denisova girl.

Until now, we knew that Neandertal mtDNA grouped together and so did modern human mtDNA. The two groups shared a Middle Pleistocene common ancestor and a much more distant common ancestor (~1 million years) with the mtDNA found in Denisova. The new Sima specimen shares descent from Denisova. This is important because it shows that whatever archaic human population the Denisovan mtDNA belonged to also extended to western Europe. And, surprisingly, the Sima specimen did not group with Neandertals, as might be expected because of the incipient Neanderthaloid morphology of the Sima hominins which has been a matter of controversy as it pushes back the evolutionary lineage of H. neandertalensis deeper into the Middle Pleistocene that some researchers accept.

Before this paper, it was believed that H. heidelbergensis evolved somewhere (perhaps Near East or Africa), a subset of it evolved to H. sapiens in Africa, and a different subset evolved in Eurasia, leading up to H. neandertalensis in the west, and unknown forms in the east, of which the Denisova girl was a matrilineal descendant. The next question is: when did Neandertals and Neandertal mtDNA appear in Europe? 

It can now be hoped that such questions will be answered directly. The Sima individual studied in this paper is not some frozen specimen from the Arctic, preserved by a freak accident in pristine form for hundreds of thousands of years, but a person who lived in Southwestern Europe. I am fairly sure that this won't be the last really old human we see a paper about in the coming years. Human mtDNA used to present a simple picture at the time of the discovery of African mitochondrial Eve: the deepest splits were in Africa and Eurasians belonged to a subset of African variation. But, as more and more archaic Eurasian mtDNA is sampled, it now appears that modern human mtDNA is a subset of world human mtDNA whose deepest splits are in Eurasia, and the next deepest splits are in Africa. Obviously, this may be a consequence of the fact that archaic human mtDNA has only been sampled from Eurasia, for factors relating to DNA preservation. But, it is nonetheless interesting to wonder where on the tree the mtDNA of archaic Africans would fall.

Nature (2013) doi:10.1038/nature12788

A mitochondrial genome sequence of a hominin from Sima de los Huesos

Matthias Meyer et al.

Excavations of a complex of caves in the Sierra de Atapuerca in northern Spain have unearthed hominin fossils that range in age from the early Pleistocene to the Holocene1. One of these sites, the ‘Sima de los Huesos’ (‘pit of bones’), has yielded the world’s largest assemblage of Middle Pleistocene hominin fossils2, 3, consisting of at least 28 individuals4 dated to over 300,000 years ago5. The skeletal remains share a number of morphological features with fossils classified as Homo heidelbergensis and also display distinct Neanderthal-derived traits6, 7, 8. Here we determine an almost complete mitochondrial genome sequence of a hominin from Sima de los Huesos and show that it is closely related to the lineage leading to mitochondrial genomes of Denisovans9, 10, an eastern Eurasian sister group to Neanderthals. Our results pave the way for DNA research on hominins from the Middle Pleistocene.

Link

Iberian Neolithic farmer DNA

A currently not available preprint that has important implications about the Neolithic of Europe.

A late Neolithic Iberian farmer exhibits genetic affinity to Neolithic Scandinavian farmers and a Bronze Age central European farmer

Sverrisdóttir, Oddný Ósk et al.

The spread of farming, the neolithisation process, swept over Europe after the advent of the farming lifestyle in the near east approximately 11,000 years ago. However the mode of transmission and its impact on the demographic patterns of Europe remains largely unknown. In this study we obtained : 66,476,944 bp of genomic DNA from the remains of a 4000 year old Neolithic farmer from the site of El Portalón, 15 km east of Burgos, Spain. We compared the genomic signature of this individual to modern-day populations as well as the few Neolithic individuals that has produced large-scale autosomal data. The Neolithic Portalón individual is genetically most similar to southern Europeans, similar to a Scandinavian Neolithic farmer and the Tyrolean Iceman. In contrast, the Neolithic Portalón individual displays little affinity to two Mesolithic samples from the near-by area, La Brana, demonstrating a distinct change in population history between 7,000 and 4,000 years ago for the northern Iberian Peninsula.

Link

Aurignacian rock art from Altxerri B cave

Journal of Human Evolution doi:0.1016/j.jhevol.2013.08.001

Not only Chauvet: Dating Aurignacian rock art in Altxerri B Cave (northern Spain)

C. González-Sainz et al.

The discovery and first dates of the paintings in Grotte Chauvet provoked a new debate on the origin and characteristics of the first figurative Palaeolithic art. Since then, other art ensembles in France and Italy (Aldène, Fumane, Arcy-sur-Cure and Castanet) have enlarged our knowledge of graphic activity in the early Upper Palaeolithic. This paper presents a chronological assessment of the Palaeolithic parietal ensemble in Altxerri B (northern Spain). When the study began in 2011, one of our main objectives was to determine the age of this pictorial phase in the cave. Archaeological, geological and stylistic evidence, together with radiometric dates, suggest an Aurignacian chronology for this art. The ensemble in Altxerri B can therefore be added to the small but growing number of sites dated in this period, corroborating the hypothesis of more complex and varied figurative art than had been supposed in the early Upper Palaeolithic.

Link

mtDNA from (non-frozen) >300 thousand year old cave bear from Sima de los Huesos

PNAS doi: 10.1073/pnas.1314445110

Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments

Jesse Dabney et al.

Abstract

Although an inverse relationship is expected in ancient DNA samples between the number of surviving DNA fragments and their length, ancient DNA sequencing libraries are strikingly deficient in molecules shorter than 40 bp. We find that a loss of short molecules can occur during DNA extraction and present an improved silica-based extraction protocol that enables their efficient retrieval. In combination with single-stranded DNA library preparation, this method enabled us to reconstruct the mitochondrial genome sequence from a Middle Pleistocene cave bear (Ursus deningeri) bone excavated at Sima de los Huesos in the Sierra de Atapuerca, Spain. Phylogenetic reconstructions indicate that the U. deningeri sequence forms an early diverging sister lineage to all Western European Late Pleistocene cave bears. Our results prove that authentic ancient DNA can be preserved for hundreds of thousand years outside of permafrost. Moreover, the techniques presented enable the retrieval of phylogenetically informative sequences from samples in which virtually all DNA is diminished to fragments shorter than 50 bp.

Link

Direct dating of El Sidrón Neandertals: 48.4+/-3.2ky BP

I sometimes wonder what will be left of the "long co-existence between AMH and Neandertals in Europe" once all the radiocarbon redating dust settles. The more interesting question is: how did AMH wipe out the Neandertals? Love or War? If recent history of encounters between populations with a clear technology differential is any guide, probably a little bit of both.

Archaeometry Volume 55, Issue 1, pages 148–158, February 2013

A NEW DATE FOR THE NEANDERTHALS FROM EL SIDRÓN CAVE (ASTURIAS, NORTHERN SPAIN)*

R. E. WOOD et al.

Torres et al. (2010) published a series of radiocarbon, AAR, ESR and OSL dates from the site of El Sidrón, northern Spain, which is notable for the discovery of the partial remains of 12 Neanderthals. Whilst the non-radiocarbon methods suggested an age beyond 32 600–46 300 years, direct radiocarbon dates on the human fossils were inconsistent, ranging between 10 000 and 50 000 bp. This study uses the ultrafiltration pre-treatment protocol to obtain a date of 48 400 ± 3200 bp (OxA-21 776) on a bone fragment and confirm the antiquity of the Neanderthal assemblage. Moreover, it demonstrates the comparability of the ultrafiltration and ninhydrin bone radiocarbon pre-treatment protocols, and highlights the need for appropriate screening methods where valuable collections with poor biomolecular preservation are sampled for collagen extraction.

Link

Sweet potato genome provides link between South America and Polynesia

The actual PNAS paper seems to be still under embargo, but here's a news story in Science about the new research:

By analyzing genetic markers specific to sweet potatoes in both modern samples of the plant and older herbarium specimens, the researchers discovered significant differences between varieties found in the western Pacific versus the eastern Pacific. This finding supports the so-called tripartite hypothesis, which argues that the sweet potato was introduced to the region three times: first through premodern contact between Polynesia and South America, then by Spanish traders sailing west from Mexico, and Portuguese traders coming east from the Caribbean. The Spanish and Portuguese varieties ended up in the western Pacific, while the older South American variety dominated in the east, which would explain the genetic differences the French team saw.

Apart from the famous Heyerdahl voyage (which has recently become the subject of a 2012 movie), there was some other research regarding the introduction of Polynesian chickens to Chile. I have not followed the genetics of that part of the world very closely, but it's my impression that such a link between Polynesia and South America has not been found in the human populations of the two regions.

La Bastida, Bronze Age Iberian fortified site

From a website dedicated to it:

La Bastida (Totana, Murcia) is one of the most important archaeological sites of Prehistory in Europe. It was inhabited about 4000 years ago in the Bronze Age, and it has a great potential to understand our past and the heritage and cultural projection of Murcia Region. 

The archaeological site is located in the Sierra Tercia, on a steep hill at  confluence of the Rambla de Lebor and Salado Cliff around 6 km west of Totana town. The four hectares of surface make it one of the most extensive sites and it can only be compared to the one that occupied the present town of Lorca.

The Argaric society was a milestone of  sedentary life, urbanism, metallurgy and political and economic inequalities. La Bastida offers a unique and exceptional opportunity to understand this key stage of our past.

From a recent press release:

La Bastida unearths 4,200-year-old fortification, unique in continental Europe 

Similar characteristics have not been observed in other constructions of the Bronze Age, with three-metre thick walls, square towers originally measuring up to seven metres, a monumental entrance and an ogival arched postern gate; a fully conserved architectural element unique in Europe in that period. 

The wall protected a city measuring 4 hectares located on top of a hill. With architectural elements reminiscent of people with Eastern styled military skills, its model is typical of ancient civilisations of the Mediterranean, such as the second city of Troy. 

... 

One of the most relevant architectural elements discovered is the ogival arched postern gate, or secondary door, located near the main entrance. The arch is in very good conditions and is the first one to be found in Prehistoric Europe. Precedents can be found in the second city of Troy (Turkey) and in the urban world of the Middle East (Palestine, Israel and Jordan), influenced by the civilisations of Mesopotamia and Egypt. This indicates that people from the East participated in the construction of the fortification. These people would have reached La Bastida after the crisis which devastated their region 4,300 years ago. It was not until some 400 to 800 years later that civilisations like the Hittites and Mycenaeans, or city-states such as Ugarit, incorporated these innovative methods into their military architecture.

Related: 4.2 kiloyear event, and El Argar.

IE-speaking West Europeans are West Asian-admixed relative to Non-IE speaking Basques

Previous ADMIXTURE experiments have shown that the Basques differ from the Indo-European speaking Europeans primarily due to a lack of a "West Asian" genetic component most strongly represented on the highlands of West Asia, from Anatolia and the Caucasus through Iran to Baluchistan. The same component is "missing" from ancient European DNA prior to 5kya, making it a good candidate for an element present in the elusive Proto-Indo-Europeans.

I wanted to test the admixture of IE-speaking populations formally, so I used threepop as implemented in TreeMix which performs a formal f3 test of admixture. According to Patterson et al. (2012):

An important feature of this test is that it definitively shows that the history of mixture occurred in population C; a complex history for A or B cannot produce negative F3(C; A,B).

A negative Z-score of the f3 test is unambiguous evidence of admixture, but a zero or positive one does not exclude it.

I report f3 statistics of the following form:

f3(A; B, West_Asian)

where West_Asian consists of 50 random individuals drawn from the K7b West_Asian component.

The full list of populations used in this experiment can be seen below. They include two sources of Basques (from the HGDP and 1000Genomes Project, from France and Spain), as well as 22 Indo-European speaking populations from Western Europe

I set A as each of the 24 populations, and calculate f3-statistics of the form f3(A; B, West_Asian) where B is any one of the remaining 23 populations. Thus, there are 24*23 = 552 f3-statistics in total, of which  2*22 = 44 are of the form f3(IE; non-IE, West_Asian).

If my conjecture is correct, then I expect:

1. the IE-speaking Europeans to show significantly negative f3(IE; non-IE, West_Asian) statistics
2. the non-IE speaking Basques to show non-negative f3(non-IE; IE, West_Asian) statistics
3. the remaining f3(IE1; IE2, West_Asian) statistics to be either negative or not, depending on different levels of West_Asian-related admixture in different IE populations associated with either the Indo-Europeans or other, later, population movements emanating from West Asia.

My expectation is confirmed by the evidence. You can see all f3 statistics in the spreadsheet. I note that:

(1) Here is a histogram of the 44 f3(IE; non-IE, West_Asian) comparisons:

42 of 44 Z-scores are negative and significant, suggesting that most  IE-speaking West European populations are West Asian-admixed relative to non-IE Basques. The two that are not, involve A='Orkney_1KG', which is a drifted island population. According to Patterson et al. (2012):

As mentioned earlier, the only case where the f3-statistic for a population that is truly admixed fails to be negative is when the population has experienced a high degree of population-specific genetic drift after the admixture occurred.

(2) All f3(non-IE; IE, West_Asian) statistics are positive. With the caveat about drift in mind, there does not seem to be any evidence that Basques are more West Asian-admixed than any other population.

(3) Here is a histogram of the 462 f3(IE1; IE2, West_Asian) statistics:

This shows evidence in differences in West_Asian admixture in some but not other IE populations. 55 of the 462 comparisons show significant evidence of admixture. These mostly involve German, French, and Italian populations vs. Iberian and British Isles ones. As mentioned above, this may reflect either the diminution of Indo-European-related West Asian ancestry across Europe, or it may be due to post-IE population movements.

Discussion

It is becoming increasingly apparent that modern Europeans are the descendants of both early Neolithic farmers, presumably from the Levant or Anatolia, as well as the indigenous Mesolithic hunter-gatherers. Neolithic ancestry has persisted most strongly in southern Europe, and in Sardinia above all. Mesolithic ancestry has persisted most strongly in northern Europe, and especially in the Baltic area; however, it is everywhere in the minority, as evidenced by the ~10-fold diminution of mtDNA haplogroup U related lineages from near 100% in the earliest samples until today.

In all probability there do not exist unmixed descendants of either early Neolithic or Mesolithic Euroeans. Intriguingly, one population that may be most strongly descended from the Mesolithic Europeans are the Saami, who possess very high levels of mtDNA haplogroup U5b. But even in their case, there is evidence of more recent influences, such as Y-haplogroup N1c.

The Saami have always been somewhat of a puzzle for prehistorians, with some attributing their physical appearance to survival of cold-adapted Paleolithic northern Europeans, while others attributing it to more recent movements from Siberia. As it is so often the case, both may have been partially right: it is now revealed that the Saami are not unique in possessing affinities with northeast Asians and Amerindians, so they are descended both from the Mesolithic northern European substratum (as evidenced by mtDNA haplogroup U5b) and from more recent Siberian peoples, and are thus positioned between east and west for more than one reason.

In the rest of Europe things were not any simpler. Both analysis of modern populations, as well as the mounting ancient DNA evidence ought to have convinced us by now that "there's something about Sardinians." It does seem to appear that this island population represents has preserved most faithfully the early Neolithic European gene pool, which, as it turns out, took its time mixing with the indigenous Mesolithic populations, since it is still evident down to the Iron Age. But, all things come to an end, and so did the domination of ancient Europe by Sardinian-like people.

In continental, and especially, northern Europe, the Neolithic inhabitants, resembling modern southern Europeans, eventually admixed with the Mesolithic foragers. A legacy of this event, as well as, possibly further incursions from the east, combined to give modern northern Europeans a greater affiliation with the east of Eurasia. But, it turns out, things were not much simpler in southern and western Europe.

The modern Basques share the East Eurasian-like admixture of continental Europeans, albeit to a smaller degree than people living in the north. They, like other Europeans are a mix of Mesolithic and Neolithic peoples. But, one thing stands out in their case: their language is not Indo-European and they live surrounded by Romance Indo-European speakers. In older times, their neighbors were Indo-European Celts, some of which have survived in places like Ireland. Further away, live Germanic peoples, some of which ventured into Iberia, without much affecting the local population. One thing is certain: the Basques can no longer be seen as unmixed descendants of Cro-Magnon man. But, if they have not continued as living fossils of Paleolithic man, then, what is to account for their linguistic peculiarity?

In the current post I make one such suggestion in the framework of my theory on the Indo-Europeanization of Europe. I showed that Basques differ from all their Romance, Celtic, and Germanic fellow West Europeans in lacking a "West_Asian" influence. I have previously investigated segments of such influence in two northern Europeans. In the future, with new instruments, such as ADMIXTOOLS, we may be able to figure out exactly when other European populations were affected by this influence. For peoples living close to West Asia (e.g., Greeks or Italians), the pattern may be obscured by recent historical contacts. But, the same will probably not be true for populations living in far Western Europe (e.g., Iberians or Irish).

If my theory is correct, then this signal will postdate the 5kya mark. By how much? It is not clear how long the Indo-Europeans of western Europe maintained themselves separately, perhaps as I have speculated, as a trading/military elite centered around metallurgy and its products. Ancient DNA research has the potential of resolving this issue by first identifying the earliest arrival of the West Asian influence, and, subsequently, detecting the first emergence of something akin to the modern population. One way or another, the cat is out of the bag, and in a the coming years many of these issues will be resolved.

Estimating admixture proportions and dates with ADMIXTOOLS (Patterson et al. 2012)

This is a very exciting new paper, both for what it has to say about human history, but also because it is accompanied by a new ADMIXTOOLS software package that contain methods to infer levels of dates of admixture between populations.

Ancient European origins

There was a tip about this paper in the recent study of Native American origins. It was suggested that northern Europeans have an excess of central/east Eurasian-related ancestry relative to Sardinians. I had noticed over a year ago that northern Europeans tended to be Asian-shifted relative to Mediterranean Europeans, and when the same effect was hinted at in the Native American paper, I set out to explore the issue in a series of posts using the f4 and f3 statistics. So it's great to finally see the formal treatment of the same subject.

Figure 9 from the paper shows a scenario envisioned by the authors as consistent with the evidence:

In my earlier post I had suggested a couple of explanations for this pattern, including an Asian-shift of the Mesolithic substratum which contributes more to northern than southern Europeans, as well as a possible influence by a northern stream of Indo-European invasion into Europe. The rolloff age estimate in the paper is:

In Figure 7e we show the rolloff results. The signal is clear enough, though noisy. We estimate an admixture date of 4150 ± 850 B.P. Our standard errors computed using a block jackknife (block size=5cM) are uncomfortably large here.  

However this date must be treated with great caution. We obtained a data set from the Illumina iControl database (http://www.illumina.com/science/icontroldb.ilmn) of ‘Caucasians’ and after curation have 1,232 samples of European ancestry genotyped on an Illumina SNP array panel. We merged the data with the HGDP Illumina 650Y genotype data obtaining a data set with 561, 268 SNPs. Applying rolloff to this sample with HGDP Karitiana and Sardinians as sources, we get a much more recent date of 2200 ± 762 years B.P.

If the admixture event was related to admixture between Neolithic and Mesolithic peoples, one might guess that the admixture date would be earlier. On the other hand, the evidence shows that down to 5,000 years ago, there were farmers in Europe who were like modern Sardinians, and hunter-gatherers who were ultra-North European (even more than current north Europeans), so fusion between incoming and resident groups was not a one-time deal when they first met. A recent mtDNA study also suggests that farmers and hunter-gatherers did not completely fuse until 4,000 years BP, after which time their distinctive mtDNA types begin to expand in unison.

In my opinion, the fusion may have been effected post-5ka after the arrival of Indo-Europeans into most of Europe. Before that time, there lived in Europe groups who had either a lot or a little Neolithic ancestry. The IE invasion acted as a shock that broke down old loyalties and brought together different groups whose focus was the new military/trading elite associated primarily with metallurgy. This invasion could have acted both as a source (in its northern stream) of East Eurasian-like ancestry, since it spread east-west and passed through territory where evidence of east Eurasian mtDNA has been turning up; but it could also have acted as a blender, creating out of the "apples and oranges" that existed in Europe prior to 5ka, a new variable mix.

In any case, the authors of the current paper discuss the Mesolithic vs. Indo-European issue:

Ancient DNA studies have documented a clean break between the genetic structure of the Mesolithic hunter-gatherers of Europe and the Neolithic first farmers who followed them. Mitochondrial analyses have shown that the first farmers in central Europe, belonging to the Linear Pottery culture (LBK), were genetically strongly differentiated from European hunter-gatherers (BRAMANTI et al., 2009), with an ‘affinity’ to present day Near Eastern and Anatolian populations (HAAK et al., 2010). More recently, new insight has come from analysis of ancient nuclear DNA from three hunter-gatherers and one Neolithic farmer who lived roughly contemporaneously at about 5000 years B.P. in what is now Sweden (SKOGLUND et al., 2012). The farmer’s DNA shows a signal of genetic relatedness to Sardinians that is not present in the hunter-gatherers who have much more relatedness to present-day northern Europeans. These findings suggest that the arrival of agriculture in Europe involved massive movements of genes (not just culture) from the Near East to Europe and that people descending from the Near Eastern migrants initially reached as far north as Sweden with little mixing with the hunter-gatherers they encountered. However, the fact that today, northern Europeans have a strong signal of admixture of these two groups, as proven by this study and consistent with the findings of (SKOGLUND et al., 2012), indicates that these two ancestral groups subsequently mixed.   

Combining the ancient DNA evidence with our results, we hypothesize that agriculturalists with genetic ancestry close to modern Sardinians immigrated into all parts of Europe along with the spread of agriculture. In Sardinia, the Basque country, and perhaps other parts of southern Europe they largely replaced the indigenous Mesolithic populations, explaining why we observe no signal of admixture in Sardinians today to the limits of our resolution. In contrast, the migrants did not replace the indigenous populations in northern Europe, and instead lived side-by-side with them, admixing over time (perhaps over thousands of years). Such a scenario would explain why northern European populations today are admixed, and also have a rolloff admixture date that is substantially more recent than the initial arrival of agriculture in northern Europe. (An alternative history that could produce the signal of Asian-related admixture in northern Europeans is admixture from steppe herders speaking Indo-European languages, who after domesticating the horse would have had a military and technological advantage over agriculturalists (ANTHONY, 2007). However, this hypothesis cannot explain the ancient DNA result that northern Europeans today appear admixed between populations related to Neolithic and Mesolithic Europeans (SKOGLUND et al., 2012), and so even if the steppe hypothesis has some truth, it can only explain part of the data.)

Another application of the new methodology is to Spain, where many analyses (including some of the Dodecad Project) have shown that the population has both a "Mediterranean" and a "North European" component. The authors date this admixture to 3,600 +/- 400 BP, and they associate it with Bell Beaker-related backflow into Iberia. However, a newer study that probably appeared when this paper was in review showed that Mesolithic Iberians were also North European-like. So, one probably does not need a special explanation for their case: the Neolithic/Mesolithic mix that occurred in Scandinavia, probably also occurred in Spain.  The 3.6ky signal for North European/Sardinian-like admixture in Spain is similar to the 4.15ky signal of North Eurasian/Sardinian  admixture in northern Europe. Both cases may reflect the same event. The authors point out that these dates are inconsistent with Visigoths and the like contributing a major portion of north European ancestry to Spain, consistent with the Ralph and Coop (2012) study. It might even be tempting to ascribe the small ~0.5k difference in the age of the signal to this later migration, or even to Celtic-related migrations, since the Celts -based on phenotypic descriptions by ancient authors- belonged to a substantial degree to the northern Europeoids.

It will certainly be interesting to study the Beaker folk's autosomal DNA in relation to European prehistory, as R1b makes its first appearance with them on the European scene. Were they the people who brought North European/East Eurasian-like ancestry into Iberia, or did the pre-existing I folk already possess it? As more ancient DNA is sampled, so will our ideas about the sequence of events be better informed. (If Iron Age people from Bulgaria were also like Sardinians, then, as they say, the plot thickens.)


Dates of admixture with rolloff

Here are a couple examples of the rolloff fit of an exponential distribution that is used to estimate dates of admixture:

First, the Uygur (790 ± 60 year ago) shows a very good fit, and interesting things were happening in Central Asia in the 13th century.

Second, Xhosa, at a similar age (740 ± 30 years ago). I don't know much about them, but Wikipedia tells me that they were part of the Nguni migration:

They migrated southwards over many centuries, with large herds of Nguni cattle, probably entering what is now South Africa around 2,000 years ago in sporadic settlement, followed by larger waves of migration around 1400 AD.

A little early sporadic settlements and a large pulse at 1,400AD may very well average to something very close to the given date.

And, here is the plot for Spain, where the signal is older (3600 ± 400) and noisier, as evidenced both by the wider reported error and the visual impression:

It will certainly be fun to apply the same method on other data. I had waited for rolloff since it was originally announced, and "good things come to those who wait". One interesting test case might be that of Anatolian Turks, where, presumably there were two episodes of admixture, one, early one in Central Asia between West and East Eurasian people, and a second, recent one, in Anatolia when Central Asian Turkic speakers admixed with some of the pre-Turkic inhabitants. Another will probably be that of ANI-ASI admixture in South Asia; the group behind this paper has presented this research in conference, so I'm guessing there's another paper on that topic as well, and, perhaps the even more mysterious admixture in the case of West Africans.

The authors also announce the Affymetrix Human Origins Array which is based on ascertainments included in the Harvard HGDP set, and which I've been occasionally using in some of my own experiments. This new chip was recently used in the South African study. A new curated version of the HGDP set that removes outliers is also announced:

We successfully genotyped the array in 934 samples from the HGDP, and made the data publicly available on August 12 2011 at ftp://ftp.cephb.fr/hgdp supp10/. The present study analyzes a curated version of this dataset in which we have used Principal Component Analysis (Patterson 2006) to remove samples that are outliers relative to others from their same populations; 828 samples remained after this procedure. This curated dataset is available for download from the Reich laboratory website (http://genetics.med.harvard.edu/reich/Reich_Lab/ Datasets.html). 

UPDATE (8 Sep 2012 ): The following discussion in smallcase is now obsolete. See f-statistics are robust to differences in sample age for details.

Addendum on the applicability of tests of admixture to samples of different age

Finally, since the authors study f-statistics with the Tyrolean Iceman, it is worthwhile to link to one of my recent posts on the topic. I've made a small figure to repeat the main argument of that post:

This shows the relationship between three populations: A, Cmod, and B. A and Cmod form a clade, and B is a group whose possible tree-violating contributions we are investigating.

Canc  is an ancient individual whose genome has been sampled and who belongs to the lineage leading up to Cmod. As such, he is missing a few thousand years of evolution (shown with the dashed line). On the left figure, Canc is very old (so he is missing a lot of evolution), while on the right, he is fairly recent (so he is missing only a little).

You can mentally slide Canc up and down its branch. As it tends to Cmod (right), then Canc will appear unadmixed, because it will have "experienced" almost as many years of evolution as A has, and will be separated by exactly the same amount of evolution from B as A does. But, as  Canc becomes older (left) and approaches the Root, then it will become much more related to B than A is, only on account of it being older. A test that compares Canc with A and B may conclude that Canc is a mixture of A and B.

Here is another way to explain this:

Let B be the allele found in group B and A be the allele in group A.
The pattern ABB means that Canc has B, and hence matches B. This is consistent with admixture from B-to-Canc if the allele B first appeared on the B branch of the tree.

But, it is also consistent with B being an allele at the Root that went to both sides of the tree: Canc is more likely to match the allele at the root (because he's older, closer to the Root) than A (who's younger, so an allele at the root has had more time to be lost due to drift, or a new one to appear through mutation).

Now, I don't think this effect has played a major role in the analyses' presented in this paper for the Iceman, because if A=North European, Canc=Iceman, and Cmod=Sardinians, then the f statistics show that it is A that is admixed with a B=Karitiana-like population. It might play a role in the Neandertal-like excess identified for the Iceman, because in that case A=Europeans, B=Vindija, and it is the Iceman that appears more admixed vis a vis living Europeans. I do think, however, on the basis of my ancestry map, that even if some of the signal is due to the proposed effect, not all of it is, since Neandertal-like segments in Oetzi tend to correspond with segments likely to be of European pre-Neolithic ancestry. And, indeed, if pre-Neolithic Europeans were indeed more Neandertal-like then that is another thing in which they may have resembled East Asians.

In any case, I do believe that some thought needs to be given to tests of admixture when either (i) one of the samples is an ancient genome, or (ii) there is some reason to think that the per annum rate of evolution has been different in two populations, which would "mimic" a closer/more distant relationship to the root. As we develop the ability to sample near 100ky-old samples, strange effects might appear if a test that does not take account of differences in sample ages is used.

Conclusion

To cap this long post, the new paper represents an exciting combination of new data, software, methods, and interpretation, that will probably give genome bloggers and all those interested in human history a lot to think about and/or play with in the coming months and years. I will certainly be unbundling and trying out the new ADMIXTOOLS suite.

UPDATE: Razib also covers this new paper.

Genetics doi: 10.1534/genetics.112.145037


Ancient Admixture in Human History

Nick Patterson et al.

Population mixture is an important process in biology. We present a suite of methods for learning about population mixtures, implemented in a software package called ADMIXTOOLS, that support formal tests for whether mixture occurred, and make it possible to infer proportions and dates of mixture. We also describe the development of a new single nucleotide polymorphism (SNP) array consisting of 629,433 sites with clearly documented ascertainment that was specifically designed for population genetic analyses, and that we genotyped in 934 individuals from 53 diverse populations. To illustrate the methods, we give a number of examples where they provide new insights about the history of human admixture. The most striking finding is a clear signal of admixture into northern Europe, with one ancestral population related to present day Basques and Sardinians, and the other related to present day populations of northeast Asia and the Americas. This likely reflects a history of admixture between Neolithic migrants and the indigenous Mesolithic population of Europe, consistent with recent analyses of ancient bones from Sweden and the sequencing of the genome of the Tyrolean ‘Iceman’. 

Link