Ancient pigs reveal a near-complete genomic turnover following their introduction to Europe

Abstract

Archaeological evidence indicates that pig domestication had begun by ∼10,500 y before the present (BP) in the Near East, and mitochondrial DNA (mtDNA) suggests that pigs arrived in Europe alongside farmers ∼8,500 y BP. A few thousand years after the introduction of Near Eastern pigs into Europe, however, their characteristic mtDNA signature disappeared and was replaced by haplotypes associated with European wild boars. This turnover could be accounted for by substantial gene flow from local European wild boars, although it is also possible that European wild boars were domesticated independently without any genetic contribution from the Near East. To test these hypotheses, we obtained mtDNA sequences from 2,099 modern and ancient pig samples and 63 nuclear ancient genomes from Near Eastern and European pigs. Our analyses revealed that European domestic pigs dating from 7,100 to 6,000 y BP possessed both Near Eastern and European nuclear ancestry, while later pigs possessed no more than 4% Near Eastern ancestry, indicating that gene flow from European wild boars resulted in a near-complete disappearance of Near East ancestry. In addition, we demonstrate that a variant at a locus encoding black coat color likely originated in the Near East and persisted in European pigs. Altogether, our results indicate that while pigs were not independently domesticated in Europe, the vast majority of human-mediated selection over the past 5,000 y focused on the genomic fraction derived from the European wild boars, and not on the fraction that was selected by early Neolithic farmers over the first 2,500 y of the domestication process.

Keywords: Neolithic; domestication; evolution; gene flow.

Fig. 1.

(A) Map representing the distribution of East Asian (blue), Near Eastern (including haplogroups mt-Y1 and mt-ArmT; yellow), European (including haplogroups mt-Italian, mt-A, mt-C, and mt-Y2; red), and Y2 (purple) haplogroups in wild boars. Black dots represent the locations of 696 modern and ancient wild boar. Haplogroup assignments were used to interpolate the underlying color distribution, which demonstrates the biogeographical boundaries of these 3 general haplogroups. (B) Large pie chart in the upper right corner of the map represents overall frequencies of these haplogroups in domestic pigs. Small pie charts on the map show the frequencies at various archeological sites/locations between 8,000 y BP and 5,100 y BP (B), between 5,099 and 180 y BP [before the Industrial Revolution and the introduction of Asian pigs in Europe (35) (C), and in modern pigs (D)]. A few samples from our datasets have been excluded from these plots; more details are provided in SI Appendix, Figs. S6 and S7.

Fig. 2.

(A) Bar plots representing the proportion of ancestry from Europe (red), the Near East (yellow), and East Asia (blue) in Eurasian wild boar genomes. (B) Bar plots depicting the proportion of Near Eastern ancestry in modern and ancient European domestic pigs. (C) PCA (excluding East Asian domestic pigs; SI Appendix, Fig. S14) showing the existence of 2 groups of ancient domestic pigs: 1 close to Near Eastern wild boar and 1 close to European wild boar.