Genetic Structure of the World's First Farmers Aug 17, 2016 21:19:53 GMT
Post by Admin on Aug 17, 2016 21:19:53 GMT
The earliest evidence for cultivation and stock-keeping is found in the Neolithic core zone of the Fertile Crescent (1, 2); a region stretching north from the southern Levant through E-Anatolia and N-Mesopotamia then east into the Zagros Mountains on the border of modern-day Iran and Iraq (Fig. 1). From there farming spread into surrounding regions, including Anatolia and later Europe, southern Asia, and parts of Arabia and N-Africa. Whether the transition to agriculture was a homogeneous process across the core zone, or a mosaic of localized domestications is unknown. Likewise, the extent to which core zone farming populations were genetically homogeneous, or exhibited structure that may have been preserved as agriculture spread into surrounding regions, is undetermined.
Ancient DNA (aDNA) studies indicate that early Aegean farmers dating to c. 6,500-6,000 BCE are the main ancestors of early European farmers (3, 4), although it is not known if they were predominantly descended from core zone farming populations. We sequenced four Early Neolithic (EN) genomes from Zagros, Iran, including one to 10x mean coverage from a well-preserved male sample from the central Zagros site of Wezmeh Cave (WC1, 7,455-7,082 cal BCE). The three other individuals were from Tepe Abdul Hosein and were less well-preserved (genome coverage between 0.6 and 1.2 x) but are around 10,000 years old, and therefore are among the earliest Neolithic human remains in the world (tables S1 and S3).
The four EN Zagros genomes form a distinct cluster in the first two dimensions of a principal components analysis (PCA; Fig. 2); they plot closest to modern-day Pakistani and Afghans and are well-separated from European hunter-gatherers (HG) and other Neolithic farmers. In an outgroup f3-test (6, 7) (figs. S17-S20) all four Neolithic Iranian individuals are genetically more similar to each other than to any other prehistoric genome except a Chalcolithic genome from NW-Anatolia (see below). Despite 14C dates spanning around 1,200 years, these data are consistent with all four genomes being sampled from a single eastern Fertile Crescent EN population.
Examination of runs of homozygosity (ROH) above 500 kb in length in WC1 demonstrated that he shared a similar ROH distribution with European and Aegean Neolithics, as well as modern day Europeans (Fig. 3A, B). However, of all ancient samples considered, WC1 displays the lowest total length of short ROH, suggesting he was descended from a relatively large HG population. In contrast, the ROH distributions of the HG Kotias from Georgia, and Loschbour from Luxembourg indicate prolonged periods of small ancestral population size (8).
We also developed a method to estimate heterozygosity Embedded Image in 1Mb windows that takes into account post-mortem damage and is unbiased even at low coverage (9) (Fig. 3C, D). The mean Embedded Image in WC1 was higher than in HG individuals (Bichon and Kotias), similar to Bronze Age individuals from Hungary and modern Europeans, and lower than ancient (10) and modern Africans. Multidimensional scaling on a matrix of centered Spearman correlations of local Embedded Image across the whole genome again puts WC1 closer to modern populations than to ancient foragers, indicating that both the mean and distribution of diversity over the genome is more similar to modern populations (Fig. 3E). However, WC1 does have an excess of long ROH segments (>1.6 Mb), relative to Aegean and European Neolithics (Fig. 3B). This includes several very long (7-16 Mb) ROH segments (Fig. 3A), confirmed by low Embedded Image estimates in those regions (Fig. 3C). These regions do not show reduced coverage in WC1 nor a reduction in diversity in other samples, with the exception of the longest such segment where we find reduced diversity in modern and HG individuals, although less extended than in WC1 (7) (Fig. 3B). This observed excess of long segments of reduced heterozygosity could be the result of cultural practices such as consanguinity and endogamy, or demographic constraints such as a recent or ongoing bottleneck (11).
The extent of population genetic structure in Neolithic SW-Asia has important implications for the origins of farming. High levels of structuring would be expected under a scenario of localized independent domestication processes by distinct populations, whereas low structure would be more consistent with a single population origin of farming or a diffuse homogeneous domestication process, perhaps involving high rates of gene flow across the entire Neolithic core zone. The ancient Zagros individuals show stronger affinities to Caucasus HGs (table S17.1) whereas Neolithic Aegeans showed closer affinities to other European HGs (tables S17.2 and S17.3). Formal tests of admixture of the form f3(Neo_Iranian, HG; Anatolia_Neolithic) were all positive with Z-scores above 15.78 (table S17.6), indicating that Neolithic NW-Anatolians did not descend from a population formed by the mixing of Zagros Neolithics and known HG groups. These results suggest that Neolithic populations from NW-Anatolia and the Zagros descended from distinct ancestral populations. Furthermore, while the Caucasus HGs are genetically closest to EN Zagros individuals, they also share unique ancestry with eastern, western, and Scandinavian European HGs (table S16.1), indicating that they are not the direct ancestors of Zagros Neolithics.
‘Chromosome painting’ and an analysis of recent haplotype sharing using a Bayesian mixture model (7) revealed that, when compared to 170-230 modern groups, WC1 shared a high proportion (>95%) of recent ancestry with individuals from the Middle East, Caucasus and India. We also compared WC1's haplotype sharing profile to that of three high coverage Neolithic genomes from NW-Anatolia (Bar8; Barcın, Fig. 4), Germany (LBK; Stuttgart) and Hungary (NE1; Polgár-Ferenci-hát). Unlike WC1, these Anatolian and European Neolithics shared ~60-100% of recent ancestry with modern groups sampled from South Europe (figs. S24, S30, S32-S37, table S22).
We also examined recent haplotype sharing between each modern group and ancient Neolithic genomes from Iran (WC1) and Europe (LBK, NE1), HG genomes sampled from Luxembourg (Loschbour) and the Caucasus (KK1; Kotias), a 4.5k-year old genome from Ethiopia (Mota) and Ust’-Ishim, a 45k-year old genome from Siberia. Modern groups from S-, C- and NW-Europe shared haplotypes predominantly with European Neolithic samples LBK and NE1, and European HGs, while modern Near and Middle Eastern, as well as S-Asian samples had higher sharing with WC1 (figs. S28-S29). Modern Pakistani, Iranian, Armenian, Tajikistani, Uzbekistani and Yemeni samples were inferred to share >10% of haplotypes with WC1. This was true even when modern groups from neighboring geographic regions were added as potential ancestry surrogates (figs. S26-S27 and table S23). Iranian Zoroastrians had the highest inferred sharing with WC1 out of all modern groups (table S23). Consistent with this, outgroup f3 statistics indicate that Iranian Zoroastrians are the most genetically similar to all four Neolithic Iranians, followed by other modern Iranians (Fars), Balochi (SE-Iran, Pakistan and Afghanistan), Brahui (Pakistan and Afghanistan), Kalash (Pakistan) and Georgians (figs. S12-S15). Interestingly, WC1 most likely had brown eyes, relatively dark skin, and black hair, although Neolithic Iranians carried reduced pigmentation-associated alleles in several genes and derived alleles at 7 of the 12 loci showing the strongest signatures of selection in ancient Eurasians (3) (tables S29-S33). While there is a strong Neolithic component in these modern S-Asian populations, simulation of allele sharing rejected full population continuity under plausible ancestral population sizes, indicating some population turnover in Iran since the Neolithic (7).
The Neolithic transition in SW-Asia involved the appearance of different domestic species, particularly crops, in different parts of the Neolithic core zone, with no single center (20). Early evidence of plant cultivation and goat management between the 10th and the 8th millennium BCE highlight the Zagros as a key region in the Neolithisation process (1). Given the evidence of domestic species movement from East to West across SW-Asia (21), it is surprising that EN human genomes from the Zagros are not closely related to those from NW-Anatolia and Europe. Instead they represent a previously undescribed Neolithic population. Our data show that the chain of Neolithic migration into Europe does not reach back to the eastern Fertile Crescent, also raising questions about whether intermediate populations in southeastern and Central Anatolia form part of this expansion. On the other hand, it seems probable that the Zagros region was the source of an eastern expansion of the SW-Asian domestic plant and animal economy. Our inferred persistence of ancient Zagros genetic components in modern day S-Asians lends weight to a strong demic component to this expansion.