Genome-wide analysis reveals artificial selection on coat colour and reproductive traits in Chinese domestic pigs

Pigs from Asia and Europe were independently domesticated from c. 9000 years ago. During this period, strong artificial selection has led to dramatic phenotypic changes in domestic pigs. However, the genetic basis underlying these morphological and behavioural adaptations is relatively unknown, particularly for indigenous Chinese pigs. Here, we performed a genome-wide analysis to screen 196 regions with selective sweep signals in Tongcheng pigs, which are a typical indigenous Chinese breed. Genes located in these regions have been found to be involved in lipid metabolism, melanocyte differentiation, neural development and other biological processes, which coincide with the evolutionary phenotypic changes in this breed. A synonymous substitution, c.669T>C, in ESR1, which colocalizes with a major quantitative trait locus for litter size, shows extreme differences in allele frequency between Tongcheng pigs and wild boars. Notably, the variant C allele in this locus exhibits high allele frequency in most Chinese populations, suggesting a consequence of positive selection. Five genes (PRM1, PRM2, TNP2, GPR149 and JMJD1C) related to reproductive traits were found to have high haplotype similarity in Chinese breeds. Two selected genes, MITF and EDNRB, are implied to shape the two-end black colour trait in Tongcheng pig. Subsequent SNP microarray studies of five Chinese white-spotted breeds displayed a concordant signature at both loci, suggesting that these two genes are responsible for colour variations in Chinese breeds. Utilizing massively parallel sequencing, we characterized the candidate sites that adapt to artificial and environmental selections during the Chinese pig domestication. This study provides fundamental proof for further research on the evolutionary adaptation of Chinese pigs.

约9000年前，亚洲与欧洲的野猪分别被独立驯化为家猪。在此驯化进程中，高强度的人工选择使家猪产生了显著的表型变化。然而，这些形态与行为适应性背后的遗传基础仍不甚明晰，针对中国地方猪种的相关研究尤为匮乏。
本研究针对中国典型地方猪种——通城猪开展全基因组分析，筛选得到196个携带选择清除（selective sweep）信号的基因组区域。富集于这些区域的基因参与脂质代谢、黑素细胞分化、神经发育等多种生物学过程，与该品种的进化表型变化高度契合。
位于雌激素受体1（ESR1）基因的同义突变c.669T>C与产仔数主效数量性状位点共定位，该突变位点的等位基因频率在通城猪与野猪间存在显著差异。值得注意的是，该位点的变异等位基因C在多数中国猪群中呈现高频率分布，提示其经历了正向选择作用。
研究发现，与繁殖性状相关的5个基因（PRM1、PRM2、TNP2、GPR149及JMJD1C）在中国猪品种中具有高度相似的单倍型。
两个受选择的基因小眼畸形相关转录因子（MITF）与内皮素受体B（EDNRB）被认为参与塑造了通城猪的两头黑毛色性状。后续针对5个中国白斑猪品种的SNP芯片分析结果显示，这两个位点呈现一致的选择信号，表明这两个基因是中国猪品种毛色变异的关键调控因子。
本研究利用大规模并行测序技术，鉴定了中国家猪驯化过程中响应人工选择与环境适应的候选位点。本研究为中国家猪进化适应性的后续研究提供了重要的理论基础。