Neolithic Aegean genomes

I had covered this paper when it went on the bioRxiv, but the final version has been published in PNAS in open access.

PNAS doi: 10.1073/pnas.1523951113

Early farmers from across Europe directly descended from Neolithic Aegeans

Zuzana Hofmanová, Susanne Kreutzer et al.

Farming and sedentism first appeared in southwestern Asia during the early Holocene and later spread to neighboring regions, including Europe, along multiple dispersal routes. Conspicuous uncertainties remain about the relative roles of migration, cultural diffusion, and admixture with local foragers in the early Neolithization of Europe. Here we present paleogenomic data for five Neolithic individuals from northern Greece and northwestern Turkey spanning the time and region of the earliest spread of farming into Europe. We use a novel approach to recalibrate raw reads and call genotypes from ancient DNA and observe striking genetic similarity both among Aegean early farmers and with those from across Europe. Our study demonstrates a direct genetic link between Mediterranean and Central European early farmers and those of Greece and Anatolia, extending the European Neolithic migratory chain all the way back to southwestern Asia.

Link

Even more Anatolian Neolithic genomes

Recently I proclaimed the problem of "Neolithization of Europe" to be "done", but it doesn't hurt to have more confirmation as this new paper does. The Anatolian data is from a different site than those used by Mathieson et al. and Hofmanová, Kreutzer et al. albeit still in the extreme northwest of Asia Minor. Nonetheless, the individual from Kumtepe doesn't seem to carry any major surprises, so "Neolithization of Europe" remains "done".

Current Biology http://dx.doi.org/10.1016/j.cub.2015.12.019

Genomic Evidence Establishes Anatolia as the Source of the European Neolithic Gene Pool 

Ayça Omrak et al.

Anatolia and the Near East have long been recognized as the epicenter of the Neolithic expansion through archaeological evidence. Recent archaeogenetic studies on Neolithic European human remains have shown that the Neolithic expansion in Europe was driven westward and northward by migration from a supposed Near Eastern origin [ 1–5 ]. However, this expansion and the establishment of numerous culture complexes in the Aegean and Balkans did not occur until 8,500 before present (BP), over 2,000 years after the initial settlements in the Neolithic core area [ 6–9 ]. We present ancient genome-wide sequence data from 6,700-year-old human remains excavated from a Neolithic context in Kumtepe, located in northwestern Anatolia near the well-known (and younger) site Troy [ 10 ]. Kumtepe is one of the settlements that emerged around 7,000 BP, after the initial expansion wave brought Neolithic practices to Europe. We show that this individual displays genetic similarities to the early European Neolithic gene pool and modern-day Sardinians, as well as a genetic affinity to modern-day populations from the Near East and the Caucasus. Furthermore, modern-day Anatolians carry signatures of several admixture events from different populations that have diluted this early Neolithic farmer component, explaining why modern-day Sardinian populations, instead of modern-day Anatolian populations, are genetically more similar to the people that drove the Neolithic expansion into Europe. Anatolia’s central geographic location appears to have served as a connecting point, allowing a complex contact network with other areas of the Near East and Europe throughout, and after, the Neolithic.

Link

Neolithic farmers from Greece and Anatolia

A couple of new papers appeared this week. First, an article in Nature on natural selection in ancient Europe includes a sample of Anatolian Neolithic farmers and concludes that the European Neolithic farmers were descended from them with a bit of extra European hunter-gatherer admixture. Second, a new preprint on the bioRxiv includes Neolithic samples from northern Greece and finds that they too resemble the Anatolian and European farmers. I think it is time to declare the problem of "Neolithization of Europe" done. It took less than 4 years to solve it with ancient DNA. Here is a (non-exhaustive) list of papers in historical review:

• Keller et al. (2012): Iceman (5kya) looks Sardinian! Was this a fluke?
• Skoglund et al. (2012): No, because... Swedish farmer (5kya) looked Sardinian too! When did these "Sardinians" come to Europe?
• Lazaridis et al. (2014): No later than an LBK farmer from Germany (7kya) but what about western Europe?
• Haak, Lazaridis et al. (2015): Spanish early farmers from northern Spain looked Sardinian too 
• Olalde, Schroeder et al. (2015): Ditto for Mediterranean Spain! So where did they all come from?
• Mathieson et al. (2015): Anatolia!
• Hofmanová, Kreutzer et al. (2015): via Greece!

Nature (2015) doi:10.1038/nature16152

Genome-wide patterns of selection in 230 ancient Eurasians

Iain Mathieson et al.

Ancient DNA makes it possible to observe natural selection directly by analysing samples from populations before, during and after adaptation events. Here we report a genome-wide scan for selection using ancient DNA, capitalizing on the largest ancient DNA data set yet assembled: 230 West Eurasians who lived between 6500 and 300 BC, including 163 with newly reported data. The new samples include, to our knowledge, the first genome-wide ancient DNA from Anatolian Neolithic farmers, whose genetic material we obtained by extracting from petrous bones, and who we show were members of the population that was the source of Europe’s first farmers. We also report a transect of the steppe region in Samara between 5600 and 300 BC, which allows us to identify admixture into the steppe from at least two external sources. We detect selection at loci associated with diet, pigmentation and immunity, and two independent episodes of selection on height.

Link

bioRxiv http://dx.doi.org/10.1101/032763

Early farmers from across Europe directly descended from Neolithic Aegeans

Zuzana Hofmanová, Susanne Kreutzer et al.

Farming and sedentism first appear in southwest Asia during the early Holocene and later spread to neighboring regions, including Europe, along multiple dispersal routes. Conspicuous uncertainties remain about the relative roles of migration, cultural diffusion and admixture with local foragers in the early Neolithisation of Europe. Here we present paleogenomic data for five Neolithic individuals from northwestern Turkey and northern Greece, spanning the time and region of the earliest spread of farming into Europe. We observe striking genetic similarity both among Aegean early farmers and with those from across Europe. Our study demonstrates a direct genetic link between Mediterranean and Central European early farmers and those of Greece and Anatolia, extending the European Neolithic migratory chain all the way back to southwestern Asia.

Link

Prehistoric farmers from northern Greece had lactose intolerance, brown eyes, dark skin

According to this:

Πολύ σημαντικό πρόσφατο εύρημα αποτελεί η ανάκτηση ολόκληρων γονιδιωμάτων από τρεις προϊστορικούς αγρότες, που έζησαν στη Βόρεια Ελλάδα 7.500 με 5.500 χρόνια πριν από σήμερα. Τα δεδομένα αυτά αναλύονται και αναμένεται να ρίξουν φως στις προγονικές σχέσεις των πρώτων Ευρωπαίων και να δώσουν πλήθος πληροφοριών, που συνδέονται με λειτουργικά και μορφολογικά χαρακτηριστικά. Ήδη, είναι γνωστό, ότι κάποιοι νεολιθικοί πρόγονοί μας δε μπορούσαν να πέψουν το γάλα, ήταν δηλαδή δυσανεκτικοί στη λακτόζη και είχαν καστανά μάτια και σκουρόχρωμη επιδερμίδα.

Related video:

Ancient mtDNA from Neolithic France

PLoS ONE 10(4): e0125521. doi:10.1371/journal.pone.0125521

When the Waves of European Neolithization Met: First Paleogenetic Evidence from Early Farmers in the Southern Paris Basin

Maïté Rivollat et al.

An intense debate concerning the nature and mode of Neolithic transition in Europe has long received much attention. Recent publications of paleogenetic analyses focusing on ancient European farmers from Central Europe or the Iberian Peninsula have greatly contributed to this debate, providing arguments in favor of major migrations accompanying European Neolithization and highlighting noticeable genetic differentiation between farmers associated with two archaeologically defined migration routes: the Danube valley and the Mediterranean Sea. The aim of the present study was to fill a gap with the first paleogenetic data of Neolithic settlers from a region (France) where the two great currents came into both direct and indirect contact with each other. To this end, we analyzed the Gurgy 'Les Noisats' group, an Early/Middle Neolithic necropolis in the southern part of the Paris Basin. Interestingly, the archaeological record from this region highlighted a clear cultural influence from the Danubian cultural sphere but also notes exchanges with the Mediterranean cultural area. To unravel the processes implied in these cultural exchanges, we analyzed 102 individuals and obtained the largest Neolithic mitochondrial gene pool so far (39 HVS-I mitochondrial sequences and haplogroups for 55 individuals) from a single archaeological site from the Early/Middle Neolithic period. Pairwise FST values, haplogroup frequencies and shared informative haplotypes were calculated and compared with ancient and modern European and Near Eastern populations. These descriptive analyses provided patterns resulting from different evolutionary scenarios; however, the archaeological data available for the region suggest that the Gurgy group was formed through equivalent genetic contributions of farmer descendants from the Danubian and Mediterranean Neolithization waves. However, these results, that would constitute the most ancient genetic evidence of admixture between farmers from both Central and Mediterranean migration routes in the European Neolithization debate, are subject to confirmation through appropriate model-based approaches.

Link

Ancient mtDNA from cis-Baikal area

Russian Journal of Genetics: Applied Research January 2015, Volume 5, Issue 1, pp 26-32

Mitochondrial DNA diversity in the gene pool of the Neolithic and Early Bronze Age Cisbaikalian human population R. O. Trapezov, A. S. Pilipenko, V. I. Molodin

This paper presents the results of a study of a mitochondrial DNA sample (N = 15) from the remains of representatives of the Neolithic and Early Bronze Age (VI–III millennia BC) Cisbaikalian human population. It was found that the mitochondrial gene pool of the ancient population under study contains lineages of East Eurasian haplogroups D, G2a C, Z, and F1b. The results of the comparative analysis of the group under study with ancient and modern Eurasian populations suggest that the development of autochtonous East Eurasian genetic components was the main mechanism of the formation of the population of the Baikal region. Genetic contacts with populations of neighboring regions of Central Asia also contributed to the formation of the gene pool of the Cisbaikalian population.

Link

Natural selection and ancient European DNA

A new preprint on the bioRxiv studies the same data as the recent Haak et al. paper, but focuses on natural selection in Europe. Until recently, selection could only be studied by looking at modern populations, but since selection is genetic change over time effected by the environment, it's possible that studies like this will be the norm in the future.

The new study seems to confirm the results of Wilde et al. on steppe groups, as the Yamnaya had a very low frequency of the HERC2 derived "blue eye" allele and a lower frequency of the SLC45A2 "light skin" allele than any modern Europeans. The Yamnaya seem to have been fixed for the other SLC24A5 "light skin" allele which seems to have been at high frequency in all ancient groups save the "Western Hunter Gatherers".

It seems that light pigmentation traits had already existed in pre-Indo-European Europeans (both farmers and hunter-gatherers) and so long-standing philological attempts to correlate them with the arrival of light-pigmented Indo-Europeans from the steppe (or indeed anywhere), and to contrast them with darker pre-Indo-European inhabitants of Europe were misguided. If anything, it seems that the "fairest of them all" were the Scandinavian hunter-gatherers, and a combination of light/dark pigmentation was also present in Neolithic farmers and Western Hunter Gatherers in various combinations.

It also seems that both the theory that lactose tolerance started with LBK farmers and the theory that it came to Europe from milk-drinking steppe Indo-Europeans were wrong, as this trait seems to be altogether absent in European hunter-gatherers, farmers, and Yamnaya, and make a very timid appearance in the Late neolithic/Bronze Age before shooting up in frequency to the present.

Another new development is the ability to predict "genetic height" from ancient DNA. I think this may be a little bit superfluous as you can predict "actual height" by measuring long bone lengths. On the other hand, actualized height depends not only on genetics but also on diet, disease, etc., so it's useful to look at genetic changes in such polygenic traits directly.

A big surprise was the presence of the derived EDAR allele in Swedish hunter-gatherers. This allele is very rare in modern Europeans and seems to have pleiotropic effects in East Asians. This raises the question why this allele (that was so successful in East Asians), never "took hold" in Europeans. One possibility is that it never provided an advantage to Europeans (I don't think anyone really knows what it's actually good for). Another is that Swedish hunter-gatherers simply didn't contribute much ancestry to modern Europeans and so the allele never got the chance to rise in frequency by much.

bioRxiv http://dx.doi.org/10.1101/016477

Eight thousand years of natural selection in Europe

Iain Mathieson et al.

The arrival of farming in Europe beginning around 8,500 years ago required adaptation to new environments, pathogens, diets, and social organizations. While evidence of natural selection can be revealed by studying patterns of genetic variation in present-day people, these pattern are only indirect echoes of past events, and provide little information about where and when selection occurred. Ancient DNA makes it possible to examine populations as they were before, during and after adaptation events, and thus to reveal the tempo and mode of selection. Here we report the first genome-wide scan for selection using ancient DNA, based on 83 human samples from Holocene Europe analyzed at over 300,000 positions. We find five genome-wide signals of selection, at loci associated with diet and pigmentation. Surprisingly in light of suggestions of selection on immune traits associated with the advent of agriculture and denser living conditions, we find no strong sweeps associated with immunological phenotypes. We also report a scan for selection for complex traits, and find two signals of selection on height: for short stature in Iberia after the arrival of agriculture, and for tall stature on the Pontic-Caspian steppe earlier than 5,000 years ago. A surprise is that in Scandinavian hunter-gatherers living around 8,000 years ago, there is a high frequency of the derived allele at the EDAR gene that is the strongest known signal of selection in East Asians and that is thought to have arisen in East Asia. These results document the power of ancient DNA to reveal features of past adaptation that could not be understood from analyses of present-day people.

Link (pdf)

mtDNA from Lengyel culture in Poland

PLoS ONE 10(2): e0118316. doi:10.1371/journal.pone.0118316

Between the Baltic and Danubian Worlds: The Genetic Affinities of a Middle Neolithic Population from Central Poland

Wiesław Lorkiewicz et al.

For a long time, anthropological and genetic research on the Neolithic revolution in Europe was mainly concentrated on the mechanism of agricultural dispersal over different parts of the continent. Recently, attention has shifted towards population processes that occurred after the arrival of the first farmers, transforming the genetically very distinctive early Neolithic Linear Pottery Culture (LBK) and Mesolithic forager populations into present-day Central Europeans. The latest studies indicate that significant changes in this respect took place within the post-Linear Pottery cultures of the Early and Middle Neolithic which were a bridge between the allochthonous LBK and the first indigenous Neolithic culture of north-central Europe—the Funnel Beaker culture (TRB). The paper presents data on mtDNA haplotypes of a Middle Neolithic population dated to 4700/4600–4100/4000 BC belonging to the Brześć Kujawski Group of the Lengyel culture (BKG) from the Kuyavia region in north-central Poland. BKG communities constituted the border of the “Danubian World” in this part of Europe for approx. seven centuries, neighboring foragers of the North European Plain and the southern Baltic basin. MtDNA haplogroups were determined in 11 individuals, and four mtDNA macrohaplogroups were found (H, U5, T, and HV0). The overall haplogroup pattern did not deviate from other post-Linear Pottery populations from central Europe, although a complete lack of N1a and the presence of U5a are noteworthy. Of greatest importance is the observed link between the BKG and the TRB horizon, confirmed by an independent analysis of the craniometric variation of Mesolithic and Neolithic populations inhabiting central Europe. Estimated phylogenetic pattern suggests significant contribution of the post-Linear BKG communities to the origin of the subsequent Middle Neolithic cultures, such as the TRB.

Link

8,000 year old wheat in Britain

Britain received farming later than most of Europe, but perhaps it received one of the products of farming well before any farmers set foot on the island. I've always wondered if news (and at least some products) of the agricultural revolution spread far and wide before the revolution itself did. Did foragers at the northwestern end of Europe hear stories of the strange new people that had already appeared 8,000 years ago on the opposite end of the continent?

Was this an isolated incident or will we be finding wheat elsewhere in pre-farming Europe? 

Science 27 February 2015: Vol. 347 no. 6225 pp. 998-1001

Sedimentary DNA from a submerged site reveals wheat in the British Isles 8000 years ago 

Oliver Smith et al.

The Mesolithic-to-Neolithic transition marked the time when a hunter-gatherer economy gave way to agriculture, coinciding with rising sea levels. Bouldnor Cliff, is a submarine archaeological site off the Isle of Wight in the United Kingdom that has a well-preserved Mesolithic paleosol dated to 8000 years before the present. We analyzed a core obtained from sealed sediments, combining evidence from microgeomorphology and microfossils with sedimentary ancient DNA (sedaDNA) analyses to reconstruct floral and faunal changes during the occupation of this site, before it was submerged. In agreement with palynological analyses, the sedaDNA sequences suggest a mixed habitat of oak forest and herbaceous plants. However, they also provide evidence of wheat 2000 years earlier than mainland Britain and 400 years earlier than proximate European sites. These results suggest that sophisticated social networks linked the Neolithic front in southern Europe to the Mesolithic peoples of northern Europe.

Link

Bronze Age mixing of multiple populations => Armenians (?)

As far as I can tell, the hypothesis of "several mixtures" comes from looking at many pairs of populations and seeing that different types of pairs seem like they mixed to make Armenians. Possibility (1) is that Armenians have multiple mixtures, and possibility (2) is that none of the sources work very well.

Hellenthal et al. did not find mixture in Armenians, but they worked with a different methodology and smaller sample size. Either, the N=173 sample size enabled detection of this admixture, or differences in methodology account for differences in conclusions. If true, the admixture dates in this paper would be some of the earliest discovered by looking at modern populations (without the help of ancient DNA).

The TreeMix analysis (Figure 4) is inconclusive about admixture from a population best represented by Neolithic Europeans. There is no plot of residuals in this figure, so this model with one migration event may not be adequate. Prior knowledge suggests that it isn't, as Pakistani and European populations have no admixture in Figure 4.

It's great that the authors will share their data!
ftp://ngs.sanger.ac.uk/scratch/project/team19/Armenian
As of this writing, the data is not "live"; it might appear when the paper is published.

bioRxiv doi: http://dx.doi.org/10.1101/015396

Genetic evidence for an origin of the Armenians from Bronze Age mixing of multiple populations

Marc Haber et al.

The Armenians are a culturally isolated population who historically inhabited a region in the Near East bounded by the Mediterranean and Black seas and the Caucasus, but remain underrepresented in genetic studies and have a complex history including a major geographic displacement during World War One. Here, we analyse genome-wide variation in 173 Armenians and compare them to 78 other worldwide populations. We find that Armenians form a distinctive cluster linking the Near East, Europe, and the Caucasus. We show that Armenian diversity can be explained by several mixtures of Eurasian populations that occurred between ~3,000 and ~2,000 BCE, a period characterized by major population migrations after the domestication of the horse, appearance of chariots, and the rise of advanced civilizations in the Near East. However, genetic signals of population mixture cease after ~1,200 BCE when Bronze Age civilizations in the Eastern Mediterranean world suddenly and violently collapsed. Armenians have since remained isolated and genetic structure within the population developed ~500 years ago when Armenia was divided between the Ottomans and the Safavid Empire in Iran. Finally, we show that Armenians have higher genetic affinity to Neolithic Europeans than other present-day Near Easterners, and that 29% of the Armenian ancestry may originate from an ancestral population best represented by Neolithic Europeans.

Link

Ancient DNA from prehistoric inhabitants of Hungary

A very interesting new article on Europe describes new data from ancient Hungary from the Neolithic to the Iron Age. It is open access, so go ahead and read it. I will update this entry with some comments after I read the paper myself.

UPDATE I (The petrous bone):

The authors write:

The endogenous DNA yields from the petrous samples exceeded those from the teeth by 4- to 16-fold and those from other bones up to 183-fold. Thus, while other skeletal elements yielded human, non-clonal DNA contents ranging from 0.3 to 20.7%, the levels for petrous bones ranged from 37.4 to 85.4% (Fig. 1).

This seems like a very exciting technical breakthrough that will increase DNA yields in future studies.

UPDATE II (PCA):

The Neolithic Hungarians are close to Sardinians (this has been replicated in study after study, so it's no longer a surprise when you find Neolithic Europeans that look like Sardinians).

What is surprising is that one KO1 Neolithic European is with the hunter-gatherers (top of the plot). At some level you would expect to find some hunter-gatherers in the earliest Neolithic communities in Europe as Europe wasn't empty land when the early farmers showed up. And KO1 appears one of those guys, "caught in the act" of first contact between the two groups.

The two Bronze Age samples are more like modern continental Europeans but not exactly like modern Hungarians. The Iron Age sample is in the no-man's land between Europe and the Caucasus and his "Asian" Y chromosome and mtDNA seems to agree that this is no ordinary European.

UPDATE III (How they looked):

I really like the visualization of hair and eye color predictions of the last two columns of the table on the right. It seems that the ancient Hungarians had mainly brown hair with more variability after 5,000 years ago. They mostly had brown eyes except three individuals.

An interesting thing is that NE7 who seems to have light hair and blue eyes is just like other Sardinian-like farmers of the Neolithic and also has the mtDNA haplogroup N1a1a1a that is ultra-typical for Neolithic people from Europe. So this is a warning not to conflate appearance with ancestry.

UPDATE IV (Y chromosomes):

As always, the supplement has many of the interesting details. Two Neolithic males were C6 which is the same "weird" haplogroup that La Brana hunter-gatherer from Spain had. Two other ones were I2a which is what Loschbour and Swedish hunter-gatherers had. Strangely, no Neolithic males had G which was found before in many Neolithic Europeans.

A new finding is that the Bronze Age individual BR2 belonged to haplogroup J2a1. I think this is the first time this has been found in ancient DNA and it falsifies the Phoenician sea-faring theory of the dispersal of this lineage.

Finally, the Iron Age Hungarian belonged to haplogroup N. I believe this was found in ancient Magyars from Hungary before, but apparently it existed there long before them.

Nature Communications 5, Article number: 5257 doi:10.1038/ncomms6257

Genome flux and stasis in a five millennium transect of European prehistory

Cristina Gamba et al.

The Great Hungarian Plain was a crossroads of cultural transformations that have shaped European prehistory. Here we analyse a 5,000-year transect of human genomes, sampled from petrous bones giving consistently excellent endogenous DNA yields, from 13 Hungarian Neolithic, Copper, Bronze and Iron Age burials including two to high (~22 × ) and seven to ~1 × coverage, to investigate the impact of these on Europe’s genetic landscape. These data suggest genomic shifts with the advent of the Neolithic, Bronze and Iron Ages, with interleaved periods of genome stability. The earliest Neolithic context genome shows a European hunter-gatherer genetic signature and a restricted ancestral population size, suggesting direct contact between cultures after the arrival of the first farmers into Europe. The latest, Iron Age, sample reveals an eastern genomic influence concordant with introduced Steppe burial rites. We observe transition towards lighter pigmentation and surprisingly, no Neolithic presence of lactase persistence.

Link

Y chromosomes and mtDNA of early farmers from Hungary

A new preprint has just appeared on the bioRxiv. It's free to read so I'll just summarize some results. First:

The haplotype of the Mesolithic skeleton from the Croatian Island Korčula belongs to the mtDNA haplogroup U5b2a5 (Dataset S3). The sub-haplogroup U5b has been shown to be frequent in pre-Neolithic hunter-gatherer communities across Europe [28–30,32,33,45,46]. 

But:

Contrary to the low mtDNA diversity reported from hunter-gatherers of Central/North Europe [28–30], we identify substantially higher variability in early farming communities of the Carpathian Basin  including the haplogroups N1a, T1, T2, J, K, H, HV, V, W, X, U2, U3, U4, and U5a (Table 1). Previous studies have shown that haplogroups N1a, T2, J, K, HV, V, W and X are most characteristic for the Central European LBK and have described these haplogroups as the mitochondrial ʻNeolithic packageʼ that had reached Central Europe in the 6th millennium BC [36,37]. Interestingly, most of these haplogroups show comparable frequencies between the STA, LBKT and LBK,

N1a is the "signature group" of the LBK based on previous publications and now it seems that it was also found in the Starcevo culture of Hungary. The mtDNA PCA plot (right) shows clearly that the Hungarian farmers are very similar to the German ones so it seems that the LBK is a direct outgrowth of the Carpathian Neolithic; some earlier models of "demic diffusion" argued that Neolithic farmers spread slowly across Europe, picking up hunter-gatherer ancestry as they went along, but now it seems that at least in the Hungary->Germany part of this journey interaction with hunter-gatherers was minimum.

mtDNA change over time in Europe is pictured in Figure 3 (left) showing a shared haplotype analysis. The Y-chromosome data genetic distance is shown on the right and shows the Balkan-Anatolian-Caucasian-Mesopotamian relationship of the early farmer Y-chromosomes. Practically, this is due to haplogroup G2a (and especially G2a2b), which has turned up in lots of ancient European farmers (including the famous Iceman):

Three STA individuals belong to the NRY haplogroup F* (M89) and two specimens can be assigned to the G2a2b (S126) haplogroup, and one each to G2a (P15) and I2a1 (P37.2) (Dataset S3, S5). The two investigated LBKT samples carry haplogroups G2a2b (S126) and I1 (M253). Furthermore, the incomplete SNP profiles of eight specimens potentially belong to the same haplogroups; STA: three G2a2b (S126), two G2a (P15), and one I (M170); LBKT: one G2a2b (S126) and one F* (M89) (Dataset S5).

I believe this is the first ancient finding of haplogroup I1 which attains a peak in modern Swedes. This might be useful to those who have tied this to Germanic migrations because of this, as it was already in Central Europe with the earliest farmers.

Interestingly:

Surprisingly, Y chromosome haplogroups, such as E1b1b1 (M35), E1b1b1a1 (M78), E1b1b1b2a (M123), J2 (M172), J1 (M267), and R1b1a2 (M269), which were claimed to be associated with the Neolithic expansion [23–25], have not been found so far in the 6th millennium BC of the Carpathian Basin and Central Europe. Intriguingly, R1a and R1b, which represent the most frequent European Y chromosome haplogroups today, have been reported from cultures that emerged in Central Europe during the 3rd/2nd millennium BC, while a basal R type has been reported from a Palaeolithic sample in Siberia [60] in agreement with a proposed Central Asian/Siberian origin of this lineage. In contrast, G2a has not been detected yet in late Neolithic cultures [42,43]. This suggests further demographic events in later Neolithic or post-Neolithic periods.

A cautionary tale against over-reliance on modern distributions to trace ancient origins.

Also:

Considering the entire set of 32 published NRY records available for Neolithic Europe thus far, the low paternal diversity is indeed quite remarkable: G2a is the prevailing haplogroup in the Central European and Carpathian Basin Neolithic, and in French and Iberian Neolithic datasets [36,40,41]. There are only two exceptions, namely one E1b1b (V13) [41] individual from the Avellaner cave in Spain (~5,000-4,500 BC), and two I2a [40] individuals from Treilles, France (~3,000 BC).

biorxiv http://dx.doi.org/10.1101/008664

Tracing the genetic origin of Europe's first farmers reveals insights into their social organization

Anna Szécsényi-Nagy et al.

Farming was established in Central Europe by the Linearbandkeramik culture (LBK), a well-investigated archaeological horizon, which emerged in the Carpathian Basin, in today's Hungary. However, the genetic background of the LBK genesis has not been revealed yet. Here we present 9 Y chromosomal and 84 mitochondrial DNA profiles from Mesolithic, Neolithic Starčevo and LBK sites (7th/6th millennium BC) from the Carpathian Basin and south-eastern Europe. We detect genetic continuity of both maternal and paternal elements during the initial spread of agriculture, and confirm the substantial genetic impact of early farming south-eastern European and Carpathian Basin cultures on Central European populations of the 6th-4th millennium BC. Our comprehensive Y chromosomal and mitochondrial DNA population genetic analyses demonstrate a clear affinity of the early farmers to the modern Near East and Caucasus, tracing the expansion from that region through south-eastern Europe and the Carpathian Basin into Central Europe. Our results also reveal contrasting patterns for male and female genetic diversity in the European Neolithic, suggesting patrilineal descent system and patrilocal residential rules among the early farmers.

Link

ISBA 2014 titles

Some interesting talks and posters from the upcoming International Symposium on Biomolecular Archaeology. I don't see any abstracts on the site (yet?) but the titles are intriguing. Some that caught my eye:

• Investigating the maternal lineage diversity from an early medieval site in Southern Italy
• Ancient mitochondrial and Y chromosomal DNA reveals the western Carpathian Basin as a corridor of the Neolithic expansion
• Ancient mitochondrial DNA from the Northern fringe of the Neolithic farming expansion in Europe sheds light on the dispersion process
• The effect of demography and natural selection on pigmentation heterogeneity in late Pleistocene and early Holocene Europeans
• The genomics of equine speciation and domestication
• Ancient population genetics: new insights on horse domestication
• Species identification and analysis of the Tyrolean Iceman's clothes using next generation sequencing of ancient DNA.
• Early evidence for the use of pottery: extending the ancient lipid record to the Pleistocene.
• Whey to go – first identification of lactose in prehistoric pottery
• Use of the earliest pottery on the Western and Eastern side of the Baltic
• The geographical distribution of the Polynesian cultural complex and its association with P33-C2a1 Y chromosomes: adding data from Aotearoa (New Zealand)
• Interdisciplinary investigation of an archaic hominin femur from the Swabian Jura (South-West Germany)
• Tracing the genetic history of farming populations of El Portalón Cave in the Sierra de Atapuerca, Spain.
• Ancient human genomes suggest three ancestral populations for present-day Europeans
• Ancient DNA from Early Neolithic farmers in Europe
• Genomic diversity and admixture in Stone-Age farmer and hunter-gatherer groups in Scandinavia
• Ancient DNA reveals the complex genetic history of the New World Arctic
• A prediction of the hybridisation potential between Hominin species using mitochondrial DNA
• Population Genomics of Vikings
• Tracing the genetic profile of Sus scrofa on Romanian territory from the Neolithic period until the Middle Ages
• The origins of the Aegean palatial civilizations from a population genetic perspective
• Ancient DNA evidence for a diversified origin of ancestor of Han Chinese

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

Dairy farming transition ~2,500 years BC in the far north of Europe

Proceedings of the Royal Society B doi: 10.1098/rspb.2014.0819

Neolithic dairy farming at the extreme of agriculture in northern Europe

Lucy J. E. Cramp et al.

The conventional ‘Neolithic package’ comprised animals and plants originally domesticated in the Near East. As farming spread on a generally northwest trajectory across Europe, early pastoralists would have been faced with the challenge of making farming viable in regions in which the organisms were poorly adapted to providing optimal yields or even surviving. Hence, it has long been debated whether Neolithic economies were ever established at the modern limits of agriculture. Here, we examine food residues in pottery, testing a hypothesis that Neolithic farming was practiced beyond the 60th parallel north. Our findings, based on diagnostic biomarker lipids and δ13C values of preserved fatty acids, reveal a transition at ca 2500 BC from the exploitation of aquatic organisms to processing of ruminant products, specifically milk, confirming farming was practiced at high latitudes. Combining this with genetic, environmental and archaeological information, we demonstrate the origins of dairying probably accompanied an incoming, genetically distinct, population successfully establishing this new subsistence ‘package’.

Link

The Mediterranean route into Europe (Paschou et al. 2014)

An interesting new (open access) paper in PNAS includes some new data from Crete, the Dodecanese, Cappadocia, and several other Greek (and a few non-Greek) populations, and proposes that the Neolithic followed an island-hopping migration into Europe. This is a study on modern populations that nicely complements the recent ancient mtDNA paper from PPNB which found an affinity to Neolithic Near Eastern populations among the modern inhabitants of Cyprus and Crete.

It is hard to imagine that there were ever any major impediments to gene flow between Anatolia and the Balkans as the Aegean islands and Hellespont are not formidable barriers to any culture with even rudimentary technology. Hopefully in the future it will become possible to look at ancient DNA from Greece and Anatolia and directly determine how the transfer of the Neolithic package into Europe took place and how much of the ancestry of modern populations stems from the Neolithic inhabitants vs. more recent shuffling of genes in either direction.

The authors also computed f3-statistics to see if populations were admixed, but found no significant evidence for it. If, for example, Dodecanesians were intermediate between mainland Greece and Anatolia they might have a negative f3(Dodecanesian; Cappadocia, Peloponnese) statistic. A negative statistic proves admixture but a positive one does not disprove it, but, in any case, there is no signal of admixture here so the results are compatible with the authors' model and probably incompatible with a recent admixture that would leave a significant negative signal (i.e., Dodecanesians/Cretans would have intermediate allele frequencies between Cappadocians and mainland Greeks).

PNAS doi: 10.1073/pnas.1320811111

Maritime route of colonization of Europe

Peristera Paschou et al.

The Neolithic populations, which colonized Europe approximately 9,000 y ago, presumably migrated from Near East to Anatolia and from there to Central Europe through Thrace and the Balkans. An alternative route would have been island hopping across the Southern European coast. To test this hypothesis, we analyzed genome-wide DNA polymorphisms on populations bordering the Mediterranean coast and from Anatolia and mainland Europe. We observe a striking structure correlating genes with geography around the Mediterranean Sea with characteristic east to west clines of gene flow. Using population network analysis, we also find that the gene flow from Anatolia to Europe was through Dodecanese, Crete, and the Southern European coast, compatible with the hypothesis that a maritime coastal route was mainly used for the migration of Neolithic farmers to Europe.

Link

Ancient mtDNA from pre-pottery Neolithic B

Figure on the left shows Fst values between the ancient PPNB population and modern populations.

PLOS Genetics DOI: 10.1371/journal.pgen.1004401

Ancient DNA Analysis of 8000 B.C. Near Eastern Farmers Supports an Early Neolithic Pioneer Maritime Colonization of Mainland Europe through Cyprus and the Aegean Islands

Eva Fernández et al.

The genetic impact associated to the Neolithic spread in Europe has been widely debated over the last 20 years. Within this context, ancient DNA studies have provided a more reliable picture by directly analyzing the protagonist populations at different regions in Europe. However, the lack of available data from the original Near Eastern farmers has limited the achieved conclusions, preventing the formulation of continental models of Neolithic expansion. Here we address this issue by presenting mitochondrial DNA data of the original Near-Eastern Neolithic communities with the aim of providing the adequate background for the interpretation of Neolithic genetic data from European samples. Sixty-three skeletons from the Pre Pottery Neolithic B (PPNB) sites of Tell Halula, Tell Ramad and Dja'de El Mughara dating between 8,700–6,600 cal. B.C. were analyzed, and 15 validated mitochondrial DNA profiles were recovered. In order to estimate the demographic contribution of the first farmers to both Central European and Western Mediterranean Neolithic cultures, haplotype and haplogroup diversities in the PPNB sample were compared using phylogeographic and population genetic analyses to available ancient DNA data from human remains belonging to the Linearbandkeramik-Alföldi Vonaldiszes Kerámia and Cardial/Epicardial cultures. We also searched for possible signatures of the original Neolithic expansion over the modern Near Eastern and South European genetic pools, and tried to infer possible routes of expansion by comparing the obtained results to a database of 60 modern populations from both regions. Comparisons performed among the 3 ancient datasets allowed us to identify K and N-derived mitochondrial DNA haplogroups as potential markers of the Neolithic expansion, whose genetic signature would have reached both the Iberian coasts and the Central European plain. Moreover, the observed genetic affinities between the PPNB samples and the modern populations of Cyprus and Crete seem to suggest that the Neolithic was first introduced into Europe through pioneer seafaring colonization.

Link

Middle Neolithic European archers from France

Am J Phys Anthropol DOI: 10.1002/ajpa.22504

Bioarchaeology of the middle Neolithic: Evidence for archery among early european farmers

Aline Thomas

This article focuses on Neolithic skeletons associated with the first monumental cemeteries of Western Europe and specifically those of the Cerny culture (Paris Basin, France). While this cultural context is an agrarian one, numerous arrowheads derived from complete hunting equipment are present in numerous graves. The goal of this work is to evaluate the morphological and pathological differences among the individuals according to the presence of arrowheads in their graves. It is postulated that those buried with such artifacts practiced archery, unlike their counterparts. Only adult males were selected for study to limit the effect of non-mechanical factors such as age- and sex-related modifications. The corpus consists of 36 males reliably identified among the 101 Cerny adults currently available. Thirteen men are associated with arrowheads. Variations in morphology and robusticity are evaluated on the basis of the external geometric properties of the appendicular skeleton. Entheseal changes to fibrocartilaginous attachment sites of upper and lower limbs are also examined. Both nonpathological skeletal adaptations and pathological indicators are consistent and reveal significant differences between the two groups compared. Functional adaptation is observed in the forearm bones and the clavicle in response to mechanical loads, and enthesopathies suggest repeated forceful use of upper limb muscles. These osteological changes specifically reflect the higher intensity upper limb activity of the men buried with arrowheads and correspond with the medical data on known archers, suggesting that this specific forceful task is linked to the practice of archery.

Link

Europeans = Neolithic farmers, Mesolithic hunter-gatherers and "Ancient North Eurasians" (etc.)

A new preprint on the bioRxiv reports ancient DNA from a Mesolithic European hunter-gatherer from Luxembourg whose mtDNA was published a few years ago and a Neolithic European LBK farmer from Germany, as well as several Mesolithic hunter-gatherers from Sweden.

The Luxembourg sample is similar to the Iberian La Brana samples and the Swedish Mesolithic samples are similar to Swedish Neolithic hunter-gatherers. The LBK farmer is similar to Oetzi and a Swedish TRB farmer and to Sardinians. The authors also study the recently published Mal'ta Upper Paleolithic sample from Lake Baikal and find that it is part of an "Ancient North Eurasian" population that also admixed into West Eurasians on top of the Neolithic/Mesolithic mix.

The authors' proposed model and admixture estimates:

It seems that the estimates go all the way to "almost pure" Early European farmer ancestry but "West European Hunter-Gatherer" and "Ancient North Eurasian" ancestry isn't found unmixed in any modern populations. The model seems to agree with Raghavan et al. that Karitiana are "Mal'ta"-admixed but also finds the most basal Eurasian ancestry in the European Neolithic farmer. The authors write:

The successful model (Fig. 2A) also suggests 44 ± 10% “Basal Eurasian” admixture into the ancestors of Stuttgart: gene flow into their Near Eastern ancestors from a lineage that diverged prior to the separation of the ancestors of Loschbour and Onge. Such a scenario, while never suggested previously, is plausible given the early presence of modern humans in the Levant25, African-related tools made by modern humans in Arabia26, 27, and the geographic opportunity for continuous gene flow between the Near East and Africa28

The Swedish/Luxembourg Mesolithic hunter-gatherers are all mtDNA-haplogroup U and Y-chromosome haplogroup I, so again no R1a/R1b in early European samples.

An interesting finding is that the Luxembourg hunter-gatherer probably had blue eyes (like a Mesolithic La Brana Iberian, a paper on which seems to be in the works) but darker skin than the LBK farmer who had brown eyes but lighter skin. Raghavan et al. did not find light pigmentation in Mal'ta (but that was a very old sample), so with the exception of light eyes that seem established for Western European hunter-gatherers (and may have been "darker" in European steppe populations, but "lighter" in Bronze Age South Siberians?), the origin of depigmentation of many recent Europeans remains a mystery. Ancient DNA continues to surprise at every turn.

UPDATE (4/4/2014): a new version of the preprint.

bioRxiv doi: 10.1101/001552

Ancient human genomes suggest three ancestral populations for present-day Europeans

Iosif Lazaridis et al.

Analysis of ancient DNA can reveal historical events that are difficult to discern through study of present-day individuals. To investigate European population history around the time of the agricultural transition, we sequenced complete genomes from a ~7,500 year old early farmer from the Linearbandkeramik (LBK) culture from Stuttgart in Germany and an ~8,000 year old hunter-gatherer from the Loschbour rock shelter in Luxembourg. We also generated data from seven ~8,000 year old hunter-gatherers from Motala in Sweden. We compared these genomes and published ancient DNA to new data from 2,196 samples from 185 diverse populations to show that at least three ancestral groups contributed to present-day Europeans. The first are Ancient North Eurasians (ANE), who are more closely related to Upper Paleolithic Siberians than to any present-day population. The second are West European Hunter-Gatherers (WHG), related to the Loschbour individual, who contributed to all Europeans but not to Near Easterners. The third are Early European Farmers (EEF), related to the Stuttgart individual, who were mainly of Near Eastern origin but also harbored WHG-related ancestry. We model the deep relationships of these populations and show that about ~44% of the ancestry of EEF derived from a basal Eurasian lineage that split prior to the separation of other non-Africans.

Link

Reconstruction of 5,500-year old "Stonehenge Man"

I don't see any mention of DNA in the article The face of prehistoric Britain: Forensic scientist uses Neolithic man's 5,500-year-old skull to create lifelike image as part of new £27m Stonehenge centre, so it's not clear whether the pigmentation attributed to "Stonehenge Man" is the artist's imagination or based on solid evidence.

From the article:

He is the star attraction of Stonehenge's new £27million modern visitor centre that has taken decades to produce. 

A Neolithic man has been brought to life after the most advanced forensic reconstruction of a face, based on a 5,500-year-old skeleton buried in a long barrow 1.5 miles from Stonehenge. 

The new face of the model, which has been carefully reconstructed to show people what life was like