Strong signatures of selection in the domestic pig genome

TLDR

Domestication of wild boar has produced dramatic phenotypic changes in domestic pigs, affecting behavior, body composition, reproduction, coat color, and stature traits linked to loci such as NR6A1, PLAG1, and LCORL. The study aimed to identify loci underlying phenotypic evolution in European domestic pigs. We performed whole‑genome resequencing of European domestic pigs to locate these loci. Selective sweep analyses identified strong signatures at three loci (NR6A1, PLAG1, LCORL) linked to back elongation and increased vertebrae, with most pigs homozygous for the same haplotype, while excess derived nonsynonymous substitutions and four KIT duplications in white pigs illustrate how both point mutations and structural changes drive rapid phenotypic evolution.

Abstract

Domestication of wild boar (Sus scrofa) and subsequent selection have resulted in dramatic phenotypic changes in domestic pigs for a number of traits, including behavior, body composition, reproduction, and coat color. Here we have used whole-genome resequencing to reveal some of the loci that underlie phenotypic evolution in European domestic pigs. Selective sweep analyses revealed strong signatures of selection at three loci harboring quantitative trait loci that explain a considerable part of one of the most characteristic morphological changes in the domestic pig—the elongation of the back and an increased number of vertebrae. The three loci were associated with the NR6A1, PLAG1, and LCORL genes. The latter two have repeatedly been associated with loci controlling stature in other domestic animals and in humans. Most European domestic pigs are homozygous for the same haplotype at these three loci. We found an excess of derived nonsynonymous substitutions in domestic pigs, most likely reflecting both positive selection and relaxed purifying selection after domestication. Our analysis of structural variation revealed four duplications at the KIT locus that were exclusively present in white or white-spotted pigs, carrying the Dominant white, Patch, or Belt alleles. This discovery illustrates how structural changes have contributed to rapid phenotypic evolution in domestic animals and how alleles in domestic animals may evolve by the accumulation of multiple causative mutations as a response to strong directional selection.