Ancient Melting pot of Near east

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New research on one history's most important trading hubs provides some of the earliest genetic glimpses at the movement and interactions of populations that lived in parts of Western Asia between two major events in human history: the origins of agriculture and the rise of some of the world's first cities.

The researchers, made up of an international team of scientists including Harvard anthropology professor Christina Warinner, looked at DNA data from 110 skeletal remains in West Asia dated 3,000 to 7,500 years ago. The remains came from archaeological sites in the Anatolia (present-day Turkey), the Northern Levant which includes countries on the Mediterranean coast such as Israel and Jordan, and countries in the Southern Caucasus which include present-day Armenia and Azerbaijan.

Based on their analysis, the scientists describe two genomic events that occurred around 8,500 years ago and 4,000 years ago that pointed to long-term genetic mixing in the region and subtle population movements within the area, shedding light on a long-standing question.

"Within this geographic scope, you have a number of distinct populations, distinct ideological groups that are interacting quite a lot and it hasn't really been clear to what degree people are actually moving or if this is simply just a high contact area from trade," said Warinner, assistant professor of anthropology at the Faculty of Arts and Sciences and the Sally Starling Seaver Assistant Professor at the Radcliffe Institute for Advanced Study. "What we can see is that rather than this period being characterized by dramatic migrations or conquest, what we see is the slow mixing of different populations, the slow mixing of ideas, and it's percolating out of this melting pot that we see the rise of urbanism -- the rise of cities,"
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The study was led by the Max Planck-Harvard Research center for the Archaeoscience of the Ancient Mediterranean and published in the journal Cell. Warinner was a senior author on the paper.

Historically, Western Asia, which includes the modern-day Middle East, is one of the world's most important geographical locations. Early on it not only created some of humanity's earliest cities but its early trade routes laid the foundation for what would become the Silk Road, a route that commercially linked Asia, Africa, and Europe.

Even prior to being connected with other regions, however, populations across Western Asia had already developed their own distinct traditions and systems of social organization and complexity. The areas studied in this paper played major roles in this development from early farming to pastoral communities to early state-level societies.

With the study, the researchers wanted to fill in some of the anthropological gaps between the origins of agriculture and of cities to better understand these different communities came together to eventually form cities.

"What we see in archeology is that the interconnectivity within Western Asia increased and areas such as Anatolia, the Northern Levant, and the Caucasus became a hub for [the] exchange of ideas and material culture," said Eirini Skourtanioti, a Ph.D. student at the Max Plank Institute and the lead author of the study, in a video accompanying the release of the paper. "The goal of our study was to understand the role of human mobility throughout this process."

The researchers included an international team of authors from many disciplines and countries, including Australia, Azerbaijan, France, Italy, Germany, South Korea, Turkey, and the United States. They gathered the 110 ancient remains and took samples from their teeth and part of the temporal bone called the petrous, which is part of the inner ear. The samples from the skeletons were all previously excavated and were housed in different museums and labs around the world. The genetic analysis was all conducted by scientists at the Max Planck Institute, including Warinner.

In the paper, the authors outline how approximately 8,500 years ago, populations across Anatolia and the Southern Caucasus began genetically mixing. It resulted in a gradual change in genetic profile that over a thousand years slowly spread across the both areas and entered into what is now Northern Iraq. Known as a cline in genetics, this mixture indicated to the researchers ongoing human mobility in the area and the development of a regional genetic melting pot in Anatolia and its surrounding areas.

The other shift researchers detected wasn't as gradual. They looked at samples from the ancient cities of Alalakh and Ebla in what is today southern Turkey and northern Syria and saw that around 4,000 years ago the Northern Levant experienced a relatively sudden introduction of new people.

The subtle genetic shifts points to a mass migration event. The timing of this migration corresponds with a massive drought in Northern Mesopotamia. It is likely where the migrants that entered the Northern Levant area originated from. The scientists can't be sure because there are currently no well preserved genomes for Mesopotamia.

Along with findings on interconnectivity in the region, the paper presents new information about long distance migration during the late Bronze age about 4,000 years ago. Researchers determined that a lone corpse, found buried in a well, genetically belonged in Central Asia at the time, not at a site that is part of present-day Turkey.

"We can't exactly know her story, but we can piece together a lot of information that suggests that either she or her ancestors were fairly recent migrants from Central Asia," said Warinner, who is also a group leader in the Department of Archaeogenetics at the Max Planck Institute. "We don't know the context in which they arrived in the Eastern Mediterranean but this is a period of increasing connectivity in this part of the world."
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The corpse had many injuries and the way she was buried indicates a violent death. Warinner hopes more genomic analysis can play some type of role in unraveling the ancient woman's story.

For Warinner, who earned her master's in 2008 and her Ph.D. in 2010 from the Graduate School of Arts and Sciences, these types of studies are proof of the insights DNA analysis can provide when more traditional clues don't tell the full story.

"What's really interesting is that we see these populations are mixing genetically long before we see clear material culture evidence of this -- so, long before we see direct evidence in pottery or tools or any of these more conventional archaeological evidence artifacts," Warinner said. "That's important because sometimes we're limited in how we see the past. We see the past through artifacts, through the evidence people leave behind. But sometimes events are happening that don't leave traces in conventional ways, so by using genetics, we were able to access this much earlier mixing of populations that wasn't apparent before."
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Even Indian researcher found some connections to early

populations of hunter-gatherers—in Eastern Anatolia in the case of Europe… and in a yet-unsampled location in the case of South Asia—began farming without large-scale movement of people into these regions. This does not mean that movements of people were unimportant in the introduction of farming economies at a later date; for example, ancient DNA studies have documented that the introduction of farming to Europe after 6500 BCE was mediated by a large-scale expansion of Western Anatolian farmers who descended largely from early hunter-gatherers of Western Anatolia.... It is possible that in an analogous way, an early farming population expanded dramatically within South Asia, causing large-scale population turnovers that helped to spread this economy within the region.

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central Anatolian Neolithic individuals (Boncuklu and Tepecik-Çiftlik), together with later (Pottery) Neolithic and Chalcolithic (Copper Age) individuals from northwest Anatolia (Barcın, Menteşe, and Kumtepe) and with early and middle Neolithic individuals from Europe, formed a distinct cluster to the exclusion of hunter-gatherers from western and eastern Europe (WHG and EHG, respectively), Sweden (SHG), and the Caucasus (CHG)

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There was noted genetic affinity between Kumtepe from northwest Anatolia and the Tyrolean Iceman from northern Italy. We found that the three Remedello individuals from Chalcolithic northern Italy , largely contemporary and possibly genetically and culturally affiliated with the Iceman, also had high affinity to Kumtepe in D statistics. A similar tendency for Kumtepe allele sharing was seen for a Chalcolithic individual from Hungary, CO1 , but was non-significant. Intriguingly, the Iceman/Remedello group was more similar to Kumtepe than to Boncuklu, Barcın, Tepecik-Çiftlik, or European Neolithic individuals. We further found that both Kumtepe and the Iceman/Remedello group carried more CHG alleles than other Neolithic populations. Current Biology
E L S E V I E R
The Demographic Development of the First Farmers in Anatolia
Gülşah Merve Kılınç, Ayça Omrak, [...], and Anders Götherström

Additional article information

Associated Data
Supplementary Materials
Summary
The archaeological documentation of the development of sedentary farming societies in Anatolia is not yet mirrored by a genetic understanding of the human populations involved, in contrast to the spread of farming in Europe [1, 2, 3]. Sedentary farming communities emerged in parts of the Fertile Crescent during the tenth millennium and early ninth millennium calibrated (cal) BC and had appeared in central Anatolia by 8300 cal BC [4]. Farming spread into west Anatolia by the early seventh millennium cal BC and quasi-synchronously into Europe, although the timing and process of this movement remain unclear. Using genome sequence data that we generated from nine central Anatolian Neolithic individuals, we studied the transition period from early Aceramic (Pre-Pottery) to the later Pottery Neolithic, when farming expanded west of the Fertile Crescent. We find that genetic diversity in the earliest farmers was conspicuously low, on a par with European foraging groups. With the advent of the Pottery Neolithic, genetic variation within societies reached levels later found in early European farmers. Our results confirm that the earliest Neolithic central Anatolians belonged to the same gene pool as the first Neolithic migrants spreading into Europe. Further, genetic affinities between later Anatolian farmers and fourth to third millennium BC Chalcolithic south Europeans suggest an additional wave of Anatolian migrants, after the initial Neolithic spread but before the Yamnaya-related migrations. We propose that the earliest farming societies demographically resembled foragers and that only after regional gene flow and rising heterogeneity did the farming population expansions into Europe occur.

Keywords: ancient DNA, archaeogenomics, Neolithic, Anatolia, population genetics, genetic diversity
Results and Discussion
The causes, effects, and mechanisms of the transition from foraging to farming in western Eurasia are key issues in understanding the development of our species, especially in understanding the development of larger, more dense, and more socially complex populations. Over the past decade, archaeogenetic studies have largely focused on processes that drove the spread of farming practices, particularly the introduction of farming and sedentism into Europe [2, 3, 5, 6, 7, 8, 9]. However, the demographic aspects of the transformation of forager communities in Southwest Asia into communities practicing substantial-scale mixed farming and the full extent of the role of Anatolian populations in the spread of farming into Europe have remained unclear. Here, we investigate human remains excavated from two different Neolithic settlements in central Anatolia, Boncuklu and Tepecik-Çiftlik, between circa (ca.) 8300 and 5800 calibrated (cal) BC to explore the demographic processes during the earliest (Aceramic) phase of the Neolithic transition, as well as the later Pottery Neolithic period in Anatolia.

Archaeological records show that the Neolithic era in Anatolia spanned more than 3,000 years—from around 9500 cal BC to around 6000 cal BC [4]. Farming practices were first established in the Fertile Crescent in the tenth and early ninth millennium cal BC [10] and in central Anatolia by 8300 cal BC [11, 12], or possibly earlier [12]. Between ca. 8000 cal BC and 6600 cal BC, farming spread west of central Anatolia, reaching the Aegean coast before 6600 cal BC and northwest Anatolia by 6600 at the latest [13, 14]. Debate exists as to whether this may have been a slow, steady process over those 1,400 years or relatively rapid between ca. 7000 and 6600 cal BC. Boncuklu, the earliest Anatolian site in our sample, and with evidence of very early crop cultivation in central Anatolia, is a small settlement mound dating between ca. 8300 and 7500 cal BC in the Aceramic Neolithic [11]. The excavators suggest that the Boncuklu community consisted of indigenous foragers who adopted small-scale cultivation and possibly experimented with animal herding alongside substantial traditional foraging practices [4, 11]. Tepecik-Çiftlik is a village with mixed and complex plant and animal exploitation practices, including notable elements of farming, located in the volcanic Cappadocian region of central Anatolia, dating between ca. 7500 and 5800 cal BC, from the latter Pre-Pottery Neolithic into the Pottery Neolithic [15, 16]. The evidence from Tepecik-Çiftlik indicates more substantial scale mixed farming relative to Boncuklu, although both hunting and gathering played a part in plant and animal exploitation. Both Boncuklu and Tepecik-Çiftlik show evidence of significant scale regional and inter-regional interactions, in the Tepecik-Çiftlik case especially with communities in the Fertile Crescent possibly related to the widespread distribution of obsidian [11, 15, 16]. The differences in subsistence patterns between these two settlements reflect a larger regional pattern seen in several other Aceramic and Pottery Neolithic sites in Anatolia [4, 13].

We investigated a total of nine ancient individuals excavated from Boncuklu (n = 4) and Tepecik-Çiftlik (n = 5) (Data S1). We generated genome sequence data from these individuals with a mean coverage between 0.03-fold and 6-fold per individual, using a combination of whole-genome capture and direct shotgun sequencing strategies (Supplemental Experimental Procedures; Table 1; Data S2; Figures S1A and S1B). We authenticated the sequence data using multiple well-established approaches (Supplemental Experimental Procedures; Data S1; Figure S1C). Mitochondrial genome coverages were between 66- and 2,379-fold (Table 1), and all five Tepecik-Çiftlik and three Boncuklu individuals carried the haplogroups previously found in Neolithic farmers in Europe (haplogroups K and N) (Table 1; Data S2; Figure S1D) [17]. One of the Boncuklu individuals carried the haplogroup U3, which has also been observed in a later northwest Anatolian (Pottery) Neolithic site, Barcın (Figure 1), and in early Neolithic European farmers [8, 17, 18], but not among Eurasian hunter-gatherers [19]. We identified four individuals as females and the other five as males (Table 1; Data S1).

Figure 1
Figure 1
Geographical Location and Timeline of Ancient Individuals Included in This Study
Table 1
Table 1
Summary Statistics of the Sequencing Data for Nine Ancient Individuals
We analyzed the new sequence data in the context of published ancient genetic variation (Figure 1). To discover the genetic affinities among ancient and modern-day individuals, we carried out principal component analysis (PCA). We calculated the principal components from 55 modern-day west Eurasian populations and projected the Boncuklu and Tepecik-Çiftlik individuals, as well as 85 published ancient individuals (Supplemental Experimental Procedures; Table S1), onto the first two principal components (Figure 2A). All individuals from the central Anatolian Neolithic, both the Aceramic Boncuklu group and the Pottery Neolithic Tepecik-Çiftlik group, were positioned within the genetic variation of present day southern European populations, consistent with outgroup f3 statistics (Figure S2; Data S3). Our central Anatolian Neolithic individuals (Boncuklu and Tepecik-Çiftlik), together with later (Pottery) Neolithic and Chalcolithic (Copper Age) individuals from northwest Anatolia (Barcın, Menteşe, and Kumtepe) and with early and middle Neolithic individuals from Europe, formed a distinct cluster to the exclusion of hunter-gatherers from western and eastern Europe (WHG and EHG, respectively), Sweden (SHG), and the Caucasus (CHG) (Figure 2A). Consistent with the PCA, D tests confirmed a clustering of Neolithic and Chalcolithic Anatolians to the exclusion of hunter-gatherers from Europe and the Caucasus. Hunter-gatherers from Europe and the Caucasus also share more alleles with their own groups than with Neolithic Anatolians (Figure S3A; Data S3). Interestingly, although geographically close, the Anatolian Neolithic populations from different time phases each formed discrete but proximate clusters in the PCA. Boncuklu individuals, representing the earliest phase of the Neolithic transition on the central Anatolian plateau, clustered tightly together, implying low genetic diversity within the population. In contrast, Tepecik-Çiftlik individuals, representing the later phase of the Neolithic in central Anatolia, were positioned at a peripheral position within the whole cluster and displayed high within-group diversity (Figure 2A). Pairwise f3 statistics between populations also showed significant differentiation between Boncuklu and Tepecik-Çiftlik populations (permutation test p < 0.05) (Data S3).

Figure 2
Figure 2
Genetic Structure and Diversity of Central Anatolian Neolithic Populations
To directly gauge levels of genetic diversity in Anatolian Neolithic populations, we calculated conditional nucleotide diversity in Boncuklu, Tepecik-Çiftlik, and Barcın, as well as in European Neolithic and hunter-gatherer populations (Data S3). Herein, we restricted the analysis to transversions identified in Yoruba as in [5] to avoid ascertainment bias, sequencing errors, and post-mortem degradation effects (Supplemental Experimental Procedures; Table S1). The Boncuklu population had remarkably low diversity relative to later ancient Anatolian populations, Tepecik-Çiftlik and Barcın, and European early Neolithic individuals from Hungary (Figure 2B). Comparison of the mean pairwise f3 statistics within populations also supported this result, with conspicuously higher genetic similarity within the Boncuklu group compared to Barcın and Tepecik-Çiftlik (Figure S3B; Data S3; 100% jackknife support). We further investigated short and intermediate runs of homozygosity (0.5–1.6 Mb); this is an indicator of historical effective population size and is expected to be influenced by geographic isolation and bottlenecks, but not recent inbreeding [20]. Our highest quality genome, Bon002 of Boncuklu, had 30% fewer such runs than the central European forager Loschbour, but 25%–40% more such runs relative to high-quality genomes from the Pottery Neolithic, Bar8 of Barcın and Stuttgart of Germany (Supplemental Experimental Procedures; Figure 2C). This supports the notion of a small ancestral population size in the Boncuklu population.

We further evaluated genetic differentiation among Boncuklu, Tepecik-Çiftlik, Barcın, European Mesolithic, and Neolithic populations by calculating Fst (Supplemental Experimental Procedures; Data S3). The results were consistent with the pattern of differentiation in the PCA; particularly, Boncuklu appeared to be distinct from both Tepecik-Çiftlik and Barcın (Fst = 0.020 and 0.030, respectively; Z > 4). A multidimensional scaling (MDS) plot summarizing pairwise Fst values revealed clustering of Tepecik-Çiftlik and Barcın with European Neolithic populations, whereas Boncuklu attained a peripheral location (Figure 2C). This peripheral location is most likely due to high genetic homogeneity and drift in Boncuklu, as such a pattern was not observed in an MDS analysis of mean f3 statistics (Figure S3C).

We next conducted ADMIXTURE analysis [21], inferring ancestral clusters from modern-day worldwide populations and estimating the ancestry proportions of each ancient individual based on the inferred ancestral cluster allele frequencies (Figures 3A and S4). With ten clusters (K = 10), ancestry proportions of all Anatolian (Boncuklu, Tepecik-Çiftlik, Barcın, Menteşe, and Kumtepe) and European Neolithic individuals consisted of two components, a “northern component” associated with European hunter-gatherers (WHG, SHG, and EHG) and found in modern-day northern Europe at highest frequency (orange), and a “southern component” found in the modern-day Middle East and North Africa (gray). Notably, Boncuklu displayed lower amounts of this “southern component” compared to individuals from Tepecik-Çiftlik and Barcın (Mann-Whitney U test, p < 0.001; Data S3), implying an influx of “southern component” alleles into late Aceramic and/or Pottery Neolithic settlements in Anatolia. This finding was also in line with higher genetic diversity in the later Neolithic Anatolian populations compared to Boncuklu (Figures 2B and 2C). D statistics results revealed genetic affinity between Caucasus hunter-gatherers (CHGs) and one of the individuals from Tepecik-Çiftlik, Tep003, which was greater than the rest of the individuals from Tepecik-Çiftlik and other Neolithic individuals from central Anatolia, northwest Anatolia, and Europe (Data S3). An admixture graph fitted by modeling gene flow from CHG to Tep003 using TreeMix [22] further confirmed the genetic relationship between Tep003 and CHG individuals (admixture proportion = 0.012, p = 0.002) (Figure S3D). These results show the buildup of genetic diversity during the development of the Neolithic in Anatolia.

Figure 3
Figure 3
Admixture Analysis and Genetic Affinities among Neolithic/Chalcolithic Populations
We next used our data to investigate a more recent case of possible regional migration. Previous work [6] had noted genetic affinity between Kumtepe from northwest Anatolia and the Tyrolean Iceman [23] from northern Italy. We found that the three Remedello individuals from Chalcolithic northern Italy [24], largely contemporary and possibly genetically and culturally affiliated with the Iceman, also had high affinity to Kumtepe in D statistics (Figure 3B; Data S3). A similar tendency for Kumtepe allele sharing was seen for a Chalcolithic individual from Hungary, CO1 [7], but was non-significant (Figure S3E; Data S3). Intriguingly, the Iceman/Remedello group was more similar to Kumtepe than to Boncuklu, Barcın, Tepecik-Çiftlik, or European Neolithic individuals. We further found that both Kumtepe and the Iceman/Remedello group carried more CHG alleles than other Neolithic populations (Figure 3C). This pattern of additional CHG allele sharing simultaneously observed in Iceman/Remedello and in Kumtepe is not mirrored in convergent allele sharing with other European hunter-gatherers

The low genetic diversity of the Boncuklu population, resembling the low diversity in European hunter-gatherers is interesting. It suggests that the population sizes at the very early stages of the Neolithic were not different from those of hunter-gatherers. Nearly 1,500 years later, Tepecik-Çiftlik and Barcın, fully established Neolithic populations practicing mixed farming (and within 200 km east and 400 km northwest of Boncuklu, respectively), were significantly more diverse . Part of this increased genetic diversity could be linked to (1) putative southern gene flow that could be related to the Aceramic Neolithic to Pottery Neolithic transition in the Neolithic Levant or could be related to widespread interactions in the late Aceramic Neolithic between central Anatolia and the Fertile Crescent in the late Pre-Pottery Neolithic B ; migration from the east related to similar factors of inter-regional exchanges ; and admixture among local populations. Southern and eastern gene flow into Tepecik-Çiftlik is consistent with the site’s presumed role as an obsidian hub and its cultural links with the Levant and might have started already before the Pottery Neolithic. For Barcın, these results are also in line with archaeological evidence indicating cultural influx from central Anatolia. This diverse Neolithic population most likely served as one of the sources for the well-documented wave of Neolithic migration to Europe

Post-Neolithic contacts between parts of Anatolia and central Europe are a matter of discussion. Genetic affinity between a Chalcolithic group in northwest Anatolia represented by Kum6 of Kumtepe and by a group represented by the Tyrolean Iceman was earlier explained by gene flow post-dating the earlier stages of the Neolithic in Europe [6]. But it has alternatively been interpreted as the Iceman representing a relic of the first migratory event from Anatolia [9]. As we have shown in this paper, individuals of the Chalcolithic Remedello group [24] from northern Italy also share strong affinity with Kumtepe. This pattern may be explained with one out of four scenarios: (1) Iceman/Remedello representing a relict population stemming from an early farmer migratory event, (2) late-Neolithic/Chalcolithic back-migration from central Europe into Anatolia, (3) a third source-population admixing with both the population represented by Iceman/Remedello and the population represented by Kumtepe, and (4) secondary late-Neolithic/Chalcolithic migration from Anatolia. Because the Iceman/Remedello group is genetically closer to Chalcolithic Kumtepe than to earlier Anatolian Neolithic populations, including Boncuklu and Barcın, the first scenario seems unlikely. The fact that both Iceman/Remedello and Kumtepe display shared drift with Caucasus hunter-gatherers, independent of the Bronze Age Yamnaya expansions [24, 28], also argues against Iceman/Remedello being a relict population. Second, as Kumtepe predates the Iceman/Remedello group by some 1,300 years, back migration is an unlikely explanation. Finally, the Tepecik-Çiftlik population shows significant affinity to the Iceman/Remedello group and Kumtepe relative to other Anatolian and European Neolithic populations (Figure 3D); but Tepecik-Çiftlik also predates Iceman/Remedello by approximately 3,000 years. This implies gene flow events from Tepecik-Çiftlik-related populations into the Kumtepe-related west Anatolian populations, as predicted by archaeological evidence

and further gene flow that reached northern Italy by the fourth millennium BC. We propose an additional, yet undescribed, gene flow process from Anatolia into Europe as a better explanation than a contribution from a hypothetical third source into Neolithic central Anatolia, Chalcolithic northwest Anatolia, and Chalcolithic central Europe. Thus, Neolithic population dynamics that initiated in the Anatolian region resulted in multiple waves of expansion and admixture in west Eurasia.
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