Strong signatures of selection in the domestic pig genome

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.

Is domestication driven by reduced fear of humans? Boldness, metabolism and serotonin levels in divergently selected red junglefowl ( Gallus gallus )

“…For example, Trut et al [3] argued that morphological, physiological and behavioural traits evolved as a complex in artificially selected foxes because of linkage or pleiotropy in genes controlling tameness, whereas Rubin et al [13] believed that the most likely explanation for domesticated colour phenotypes is independent selection specifically for each desired trait. Our results suggest that tameness may be a driving factor for the domesticated phenotype.…”

The ‘heritability’ of domestication and its functional partitioning in the pig

“…The most significant one was on SSC4, 82.37-82.39 Mb. This region does not contain any known gene but is close to gene PLAG1 (SSC4: 82, 606, 862-82, 608, 850 bp), which is under strong selection in European domestics (Rubin et al, 2012;Frantz et al, 2015). To contrast these results, we carried a 100 kb genomewide analysis with our approach and we found that the window containing PLAG1, made up of 891 SNPs, has a h 2 G = 0.69; this is the 493 largest heritability out of the 23 395 windows analyzed (2% upper distribution of h 2 G ).…”

“…In pigs, Rubin et al (2012) used complete genome sequence with the purpose of studying domestication. These authors combined both pool and individual sequencing and used an excess of homozygosity in domestic breeds as a proxy for selection targets.…”

“…Most of the sample sequences were downloaded from the short read archive (SRA, http://www. ncbi.nlm.nih.gov/sra; Groenen et al, 2012;Rubin et al, 2012;Esteve-Codina et al, 2013;Molnár et al, 2014;Ai et al, 2015;Bianco et al, 2015), but five were specifically sequenced for this study: a wild boar from East Russia (Primorsky Krai Peninsula, WA6), a Tunisian wild boar (WE8), a Spanish wild boar from North Spain (Asturias region, WE6) and 2 Iberian pigs (IB2 and IB3). Supplementary Table 1 presents details from all samples analyzed.…”

Mining the pig genome to investigate the domestication process

“…Second, signals of selective sweeps are expected around strongly implicated loci associated with desired phenotypic traits (for example, Wright et al, 2005). Under this hypothetical framework, researchers have attempted to identify signals of selective sweeps in domesticated specimens that are not observed in wild populations (for example, Wright et al, 2005, Rubin et al, 2012, Wilkinson et al, 2013. A number of methods have been used to detect candidate regions, including analyses of population differentiation (for example, Beaumont and Balding, 2004;Foll and Gaggiotti, 2008;Green et al, 2010), excess homozygosity and differences in linkage disequilibrium (for example, Sabeti et al, 2002;Voight et al, 2006;Tang et al, 2007), and decreased variability and skewed spectrum frequency patterns (for example, Tajima, 1989;Braverman et al, 1995;Fay and Wu, 2000;Rubin et al, 2010).…”