Genomic evidence for human-mediated introgressive hybridization and selection in the developed breed

Abstract

Background: The pig (Sus Scrofa) is one of the oldest domesticated livestock species that has undergone extensive improvement through modern breeding. European breeds have advantages in lean meat development and highly-productive body type, whereas Asian breeds possess extraordinary fat deposition and reproductive performance. Consequently, Eurasian breeds have been extensively used to develop modern commercial breeds for fast-growing and high prolificacy. However, limited by the sequencing technology, the genome architecture of some nascent developed breeds and the human-mediated impact on their genomes are still unknown.

Results: Through whole-genome analysis of 178 individuals from an Asian locally developed pig breed, Beijing Black pig, and its two ancestors from two different continents, we found the pervasive inconsistent gene trees and species trees across the genome of Beijing Black pig, which suggests its introgressive hybrid origin. Interestingly, we discovered that this developed breed has more genetic relationships with European pigs and an unexpected introgression from Asian pigs to this breed, which indicated that human-mediated introgression could form the porcine genome architecture in a completely different type compared to native introgression. We identified 554 genomic regions occupied 63.30 Mb with signals of introgression from the Asian ancestry to Beijing Black pig, and the genes in these regions enriched in pathways associated with meat quality, fertility, and disease-resistant. Additionally, a proportion of 7.77% of genomic regions were recognized as regions that have been under selection. Moreover, combined with the results of a genome-wide association study for meat quality traits in the 1537 Beijing Black pig population, two important candidate genes related to meat quality traits were identified. DNAJC6 is related to intramuscular fat content and fat deposition, and RUFY4 is related to meat pH and tenderness.

Conclusions: Our research provides insight for analyzing the origins of nascent developed breeds and genome-wide selection remaining in the developed breeds mediated by humans during modern breeding.

Keywords: Developed breed; Genetic structure; Introgression; Modern breeding; Pig; Selection.

Fig. 1

Population genetic structure of Beijing Black pig. (a) Principle component analysis for the first two PCs of 10 pig breeds. (b) Neighbor-joining phylogenetic tree constructed from SNV data among 10 populations. (c) Structure analysis with K assumed ancestral groups (K = 2–5)

Fig. 2

Pervasive inconsistent in gene-tree phylogenies. (a) Phylogenetic topologies and the corresponding numbers, the number for Topology II was significantly more (P = 2.09e-13) than that for Topology III. (b) Simulations under solely ILS scenario. The red arrow indicates the observed ratio (Topology III/Topology II) from 30,066 ortholog groups. The blue bars are a histogram of the ratios obtained under the ILS scenario. The solely ILS hypothesis was strongly rejected due to a significant difference (P < 2.2e-16) between observed and simulated ratios. (c) Individual ancestry for Beijing Black pig population using the supervised method

Fig. 3

Shenxian-pig genome introgression into Beijing-Black-pig and high similarity genomic regions of Beijing-Black-pig to Yorkshire. Blue lines display introgression from Shenxian pig to Beijing black pig across the genome. Black lines display high similarity genomic regions of Beijing Black pig to Yorkshire

Fig. 4

Distribution of regions in the genome where Beijing Black pig contains introgressed haplotypes from Yorkshire. (a) X-axis represents 18 autosomes, and the y-axis represents the relative frequency of Beijng Black pig haplotypes IBD with Shenxian pig or Yorkshire, ranging from − 1 to 1. The dotted line represents the threshold for extreme IBD with Yorkshire compared with Shenxian pig. (b) Distribution of the relative proportion of IBD haplotypes in Beijing Black pig and Shenxian pig (red, -1 to 0) or Yorkshire (blue, 0 to 1) in bins of 10,000 bp. (c) Distribution of the rIBD scores for Beijing Black pig haplotypes. (d) Z-transformed distribution of rIBD. The red line represents the threshold for extreme IBD with Yorkshire compared with Shenxian pig

Fig. 5

Selection signatures and protein structure prediction of Beijing black pig. (a) Genome-wide distribution of selection signatures detected by PBS. X-axis represents 18 autosomes, and Y-axis represents PBS statistic values. Red line displays the threshold level of 5%. (b) Prediction of protein conformation space for RUFY4 generated by missense SNV (rs322504869)

Fig. 6

Manhattan plots and Q-Q plots for meat traits GWAS of Beijing Black pig. (a): IMF content; (b): protein content; (c): pH 24 h