Genetic Structure of the World's First Farmers


90 Results
91 Patterns of genomic diversity along the Danubian corridor
92 The genetic structure and affinities of ancient individuals
93 Both multidimensional scaling (MDS) performed on the neutral portion of ancient and modern
94 genomes (Fig. 2a) and an admixture analysis (Fig. S21) revealed three main clusters of ancient
95 samples, which are found overall much more differentiated than modern individuals of SW
96 Asia and Europe: i) a cluster of European HGs, ii) a cluster of Early Neolithic individuals from
97 Iran, here represented by a single genome from Wezmeh Cave, WC1, and iii) a cluster with all
98 other Holocene individuals. In keeping with previous analyses based on a restricted set of
99 SNPs26,27, this MDS analysis (Fig. 2a) suggests strongest affinities of European and NW
100 Anatolian Neolithic samples with modern Sardinians, with the exception of the Early Neolithic
101 NW Anatolian individual Bar8 found to be closer to modern individuals from Greece, Albania
102 and other individuals from Southern Europe. However, a MDS analysis performed on the
103 whole genome including sites potentially affected by selection (Fig. S19) rather suggests that
104 early farmers are closer to Southern Europeans other than Sardinians. The Early Neolithic
105 individual from Iran (WC1) shows strongest genetic affinities with modern Iranians (Fig. 2a),
106 and to a lesser extent with individuals from the Northern Caucasus, suggesting some genetic
107 continuity in Iran since Neolithic times. Finally, Palaeolithic and Mesolithic HGs are generally
108 distinct from all modern SW Asians and Europeans, the closest of whom are Baltic Sea
109 individuals, Russians and Scandinavians.



Figure 3 - Demographic scenario inferred from the sampled genomes and underlying genetic data. a: This demographic history was obtained by summarizing the best models of all tested scenarios. b: zoom-in on the red-square area in panel a. The X symbols indicate very strong bottlenecks that occurred on the HG ancestral branch before the divergence between Bichon-Loschbour and central European HGs and some 200 kya in the ancestral population. Only admixtures with point estimates ≥ 5% are represented with arrows (≥ 10% when arrows have a dark outline). c: MDS analyses performed on the neutrally evolving portion of the 17 ancient whole-genomes used in the demographic models (left) or on data simulated (right) according to the inferred ML parameters of the global scenario shown in panes a and b.


110 Early farmers are genetically more diverse and decline in stature over time
111 While genetic diversity as quantified by the heterozygosity at neutral sites was much reduced
112 in HGs, most Early Neolithic farmers show diversity levels only slightly lower than those of
113 modern humans (Fig. 2b), with genomes from NW Anatolia at the lower end of the
114 distribution17. We note a slight reduction of diversity in modern humans with distance from
115 Anatolia to the West of Boncuklu (Spearman’s ⍴ = -0.344, p-value = 0.028), but not to the East
116 (Spearman’s ⍴ = 0.019, p-value = 0.929), while no such simple trend is observed among early
117 European farmers.

118 Compared to the other samples, the HG genomes, and in particular Bichon and SF12, show a
119 larger proportion of short (2-10Mb) Runs of Homozygosity (ROHs, Fig. 2c), in keeping with
120 previous results17,28,29. This is indicative of higher levels of remote inbreeding within European
121 by MSMC2 analyses (Fig. S25).

122 Among early farmers, WC1, Bon002, AKT16, STAR1 and Stuttgart also show a high
123 proportion of short ROHs and seem to be drawn from small populations, too. Furthermore,
124 WC1, Stuttgart, LEPE52, Bichon and Loschbour, as well as several modern individuals from
125 the Near East, carry some very long ROHs (>10Mb), indicative of recent inbreeding between
126 close relatives (potentially second cousins or closer30, Fig. S20).

127 We find that the vast majority of early farmers in our dataset had intermediate to light skin
128 complexion, while HGs had a darker skin tone (Supp. Table 3). A dark (brown to black) hair
129 color was inferred for all but two samples, LEPE52 and VC3-2, who likely had light brown
130 hair. Eye color variation was similarly low, with all samples showing high probabilities for
131 brown eyes, except for two individuals of the Starčevo culture (STAR1 and VC3-2) which
132 were likely blue-eyed.

133 Based on polygenic scores, we show that early farmers are shorter than HGs (Student t-test, t
134 = -2.427, p-value = 0.027), and their stature declined between 8,300 and 7,000 BP (Pearson's r
135 = 0.6537, p-value < 0.008, Fig. S24), suggesting that selection for short stature occurred during
136 the Neolithic expansion along the Danubian corridor.

137 The allele associated with lactase persistence was not found in any of the analyzed ancient
138 samples, consistent with an increase in frequency of these alleles at a later stage31. However,
139 early farmers already show allele frequencies similar to contemporary Europeans for 6 out of
140 7 SNPs of the FADS1/2 gene complex, potentially selected in populations with plant-based
141 diet32,33 (see Suppl. Information - Section 5, Table S7).