Archaeogenomic analysis of the first steps of Neolithization in Anatolia and the Aegean

Abstract

The Neolithic transition in west Eurasia occurred in two main steps: the gradual development of sedentism and plant cultivation in the Near East and the subsequent spread of Neolithic cultures into the Aegean and across Europe after 7000 cal BCE. Here, we use published ancient genomes to investigate gene flow events in west Eurasia during the Neolithic transition. We confirm that the Early Neolithic central Anatolians in the ninth millennium BCE were probably descendants of local hunter-gatherers, rather than immigrants from the Levant or Iran. We further study the emergence of post-7000 cal BCE north Aegean Neolithic communities. Although Aegean farmers have frequently been assumed to be colonists originating from either central Anatolia or from the Levant, our findings raise alternative possibilities: north Aegean Neolithic populations may have been the product of multiple westward migrations, including south Anatolian emigrants, or they may have been descendants of local Aegean Mesolithic groups who adopted farming. These scenarios are consistent with the diversity of material cultures among Aegean Neolithic communities and the inheritance of local forager know-how. The demographic and cultural dynamics behind the earliest spread of Neolithic culture in the Aegean could therefore be distinct from the subsequent Neolithization of mainland Europe.

Keywords: Neolithic; acculturation; ancient DNA; archaeogenomics; migration; population genetics.

Figure 1.

Genetic differentiation among ancient west Eurasians and predicted admixture events. (a,c) Results of the same multidimensional scaling (MDS) analysis, summarizing f₃-statistics (shared genetic drift) between ancient population pairs (electronic supplementary material, table S2). The goodness of fit was estimated as 0.17 and 0.17 for both dimensions. Admixture events among gene pools inferred using D-statistics are represented as arrows on each MDS plot. The circles where the arrow tips touch indicate which population is involved in the inferred admixture. Tepecik-Çiftlik is labelled as Tepecik. (a) Admixture in Boncuklu (central Anatolian PPN). For clarity, the other Anatolian/Aegean populations are not plotted. Arrow ‘a’: gene flow between Boncuklu and pre-Neolithic populations of mainland Europe (relative to other gene pools). Arrow ‘b’: gene flow between Boncuklu and the Levant populations (relative to other gene pools). Arrow ‘c’: gene flow between Boncuklu and Caucasia/Iran populations (relative to other gene pools). (b) Results of D-statistics in the form of D(Yoruba, p1; p2, Boncuklu). Multiple testing correction was performed using the Benjamini–Yekutieli method [55]. (c) Arrow ‘d’: estimated gene flow between Boncuklu and the Levantine populations. This is based on testing the topology D(Outgroup, Boncuklu; Levant_preNeolithic, Levant_Neolithic), showing that the Boncuklu population showed higher genetic affinity to the Levantine Neolithics (sample ages: ca 8300–6750 cal BCE) than to the Levantine pre-Neolithics (sample ages: ca 11 840–9760 cal BCE), although the result was only marginally significant (p > 0.05, Z > 2.5) (electronic supplementary material, figure S2c, table S5). Arrow ‘e’: gene flow from the Iran PPN population into Anatolian/Aegean PN populations. Arrow ‘f’: gene flow from the Levant PPN population into Anatolian/Aegean PN populations (electronic supplementary material, table S5 and table S6).

Figure 2.

Summary of D-statistics describing population relationships within the Anatolian/Aegean gene pool and between Anatolians/Aegeans and neighbouring groups. The Yoruba genome was used as outgroup in D-statistics. The Tepecik-Çiftlik is labelled as Tepecik. All D-statistics results are reported in electronic supplementary material, tables S8–S13. (a) D-statistics results summarized as arrows on the MDS plot (same as figure 1). Each triple population compared in D-tests is framed in the same colour. If a test population has greater genetic affinity to the second population compared to a third one, an arrow with same colour as the frames is drawn from the test population to the second population (the arrows' direction or lengths are not representative of gene flow magnitudes). Arrow ‘a’ and navy frames summarize D(Yoruba, Natufian; centralAnatolian, northAegean), where Natufians had stronger genetic affinity to north Aegean PN than to central Anatolian PPN or PN groups (electronic supplementary material, table S8). Arrows ‘b’ and ‘c’ and green frames summarize D(Yoruba, CHG&Iran_Neolithic; northAegean, centralAnatolian). In six of eight comparisons CHGs and Iran PPN populations had stronger genetic affinity to the north Aegean PN than to central Anatolian PPN and PN (electronic supplementary material, table S9). Arrow ‘d’ and purple frames summarize D(Yoruba, WHG; northAegean, centralAnatolian). In all comparisons WHGs had stronger genetic affinity to the north Aegean PN than to central Anatolian PPN and PN, with the exception of D(Yoruba, WHG; Boncuklu, Barcın) being non-significant (electronic supplementary material, table S10). (b) Results of D-tests calculated as D(Outgroup, RightPopulation; BottomPopulation, LeftPopulation), where right, bottom and left refer to the positions of the populations on the matrix. For instance the top row shows that Boncuklu has significantly higher affinity to Barcın than to Tepecik-Çiftlik. The D-statistic magnitude is represented by colour, Z score by size, and significance by being filled or not. Multiple testing correction was performed using the Benjamini–Yekutieli method [55] (electronic supplementary material, table S12 and S13).