A Comparative Study Of The Domestication Patterns In Chinese And European Pig Domestication

Since 10,000 BC, continuous human selection has led to intense genetic and phenotypic changes in pig (Sus scrofa) domestication. The phenotypic changes include a series of morphological (for example, teeth size and skull shape), behavioral (less aggressive, etc), and physiological (increased growth and prolificacy, etc) changes satisfying human needs. China and Europe, as the two main centers for pig domestication, both have a long history of pig domestication for several thousands years. Taihu, Jinhua, Rongchang, Min, Xiangzhu et al. are representatives of Chinese domestic (CHD)pig, while European domestic pigs (EUD) are represented by commercial breeds such as Duroc,Landrace, Pietrain et al. Both CHD and EUD might have been selected for these traits thereby showing increased growth and prolificacy compared to their wild ancestors. Meanwhile, both CHD and EUD are apparently less aggressive and more adaptive to domestication condition. On the other hand, different human preferences in breeding strategies could result in distinct traits in different domestic breeds. CHD are generally of higher amount of fat, stronger resistance to diseases, and better reproduction traits, while EUD, especially for the typical commercial breeds, are renowned for longer body size, rapid growth and superior leanness. So it is of value to investigate the genetic basis behind the phenotype.In this study, we analyzed worldwide samples of domestic and wild pigs, utilizing whole genome resequencing data of 263 individuals. All individuals are divided into five groups: EUD group,including 97 individuals from four typical commercial domestic breeds of Duroc, Landrace, Yorkshire(Large White) and Pietrain; European wild boar (EUW) group, including 34 individuals of European wild boar; a CHD group, comprising 81 individuals representing 14 geographically diverse breeds across China; and Chinese wild boar (CHW) group, comprising 31 individuals, including wild boars in South and North China, as well as wild boars in Korea. Finally, Sus verrucosus, Sus cebifrons, Sus celebensis, Phacochoerus africanus, Sus barbatus, Sumatran wild boars and Tibet pigs serve as an outgroup. SNP calling was performed for each group, using GATK best practice pipeline after mapping sequencing reads to the reference genome. We finally obtained 94 million SNPs in total.Based on these SNP loci,a comprehensive analysis was carried out to investigate the population structure and genetic features in multiple breeds.Based on the above data, the demographic histories for multiple pig breeds were inferred.Considering the observed correlation of demographic histories between human and pigs, we found that human activities could have exerted a great impact on the effective pig population size even before the pig domestication. Meanwhile, we inferred the domestication times in China and Europe,respectively, confirming that there is no evident bottleneck during the pig domestication.Furthermore, we combined the SNP-based analysis and haplotype-based analysis. By using Fixation index and haplotype homozygosity, we systematically investigated and compared the domestication patterns between the Chinese domestic and European domestic pigs. We identified a series of candidate genes that are crucial in the pig domestication. Consistent with the phenotypic changes, convergent and divergent genetic changes were also detected in the pig genome during domestication. We found that human mediated unidirectional selection and bidirectional selection laid the foundation for the convergent and divergent changes in domestic breeds. 31 genes, representing fundamental domestication requirements or common human needs, were identified in convergent genetic changes driven by unidirectional selection, belonging predominantly to categories related to the nervous system, muscle development, and especially to metabolic diseases. In addition, 35 genes,representing different human breeding strategies, were found under bidirectional selection for the distinct leanness and reproduction trait between CHD and EUD.Additionally, whole genome bisulfite sequencing and RNA-seq were used to validate the functional effects of genetic changes. Using ITPR3, AHR and NMU as examples, we explored and validated how the genetic variations contribute to the phenotype changes. At last, a large number of RNA-seq data were collected from public database for 21 different tissues. We conducted long intergenic non-coding RNA (LincRNA) identification in these tissues. About 17,000 LincRNAs were identified in pigs and their features are similar to the LincRNA in mouse and human. The selected LincRNA tend to have a wider expression pattern across tissues.In summary, we comprehensively investigated and compared the domestication patterns between CHD and EUD by analyzing high-throughout sequencing data. We showed that both unidirectional selection and bidirectional selection laid the foundation for the convergent and divergent changes in domestic breeds. This study provides significant insights into the pig domestication and animal evolution. The functional variants validated in the study may also provide clues to precise animal breeding and human disease research.