Archaeogenetic analysis of Neolithic sheep from Anatolia suggests a complex demographic history since domestication

Abstract

Sheep were among the first domesticated animals, but their demographic history is little understood. Here we analyzed nuclear polymorphism and mitochondrial data (mtDNA) from ancient central and west Anatolian sheep dating from Epipaleolithic to late Neolithic, comparatively with modern-day breeds and central Asian Neolithic/Bronze Age sheep (OBI). Analyzing ancient nuclear data, we found that Anatolian Neolithic sheep (ANS) are genetically closest to present-day European breeds relative to Asian breeds, a conclusion supported by mtDNA haplogroup frequencies. In contrast, OBI showed higher genetic affinity to present-day Asian breeds. These results suggest that the east-west genetic structure observed in present-day breeds had already emerged by 6000 BCE, hinting at multiple sheep domestication episodes or early wild introgression in southwest Asia. Furthermore, we found that ANS are genetically distinct from all modern breeds. Our results suggest that European and Anatolian domestic sheep gene pools have been strongly remolded since the Neolithic.

Fig. 1. Map of archaeological sites.

Geographic origins of samples from six Anatolian archaeological sites studied in the present work (see Supplementary Note 2 for details) and one Kyrgyzstan archaeological site from Taylor et al. are shown in black. Four additional Neolithic Anatolian sites relevant for sheep domestication discussed in the text are shown in red. The putative domestication center is depicted by the shaded area (adopted from Zeder).

Fig. 2. Genomic variation of modern breeds, Anatolian Neolithic (ANS) and Obishir V (OBI) sheep.

The graph represents the first two components of a PCA calculated using genotypes of 18 modern sheep breeds (n = 643). The four Anatolian Neolithic sheep individuals’ genotypes (black triangles) and three Obishir V sheep individuals’ genotypes (gray circles) were projected on these two components. Parentheses indicate the proportion of variance explained by the relevant component.

Fig. 3. Genetic similarity between ANS, OBI, and present-day sheep populations.

Outgroup f₃-statistics were used to measure similarity between (a) ANS and present-day breeds, calculated as f₃(Argali; ANS, Modern), using the joint allele frequencies of the four ANS individuals, (b) OBI and present-day breeds, calculated as f₃(Argali; OBI, Modern), using the joint allele frequencies of the three OBI individuals. The dots indicate the locations of present-day breeds (Supplementary Table 1). Redder tones reflect higher f₃ values, which indicate higher shared drift (i.e., higher similarity) between ancient and modern-day sheep. See also Supplementary Fig. 13 for outgroup f₃-statistics calculated per ANS individual.

Fig. 4. Change in mitochondrial lineages from Epipaleolithic to present-day in Anatolia.

Distribution of different haplogroups (HPG) (indicated by colors) of the studied sheep individuals. Color coding is as follows: HPG A (red), HPG B (blue), HPG C (yellow), HPG D (green), and HPG E (orange). The hatched pattern indicates individuals supported by a single sequence. Note that different periods and haplogroups are not homogeneously represented across different sites from a single region: e.g., >7500 BCE in central Anatolia is represented by Pınarbaşı and Boncuklu Höyük, while 7500–7000 BCE by Canhasan III. See Supplementary Data 1 for full details. For the samples with ages straddling two periods, we used their mean age to place them within an archaeological period. Haplogroup compositions of present-day breeds of Turkey were represented by Akkaraman (central Anatolia) and by Sakız and Kıvırcık (west Anatolia) (see Supplementary Table 4). Mitochondrial DNA haplotypes of ancient individuals are represented in Supplementary Fig. 17.