Whole-genome sequence analysis unveils different origins of European and Asiatic mouflon and domestication-related genes in sheep

Ze-Hui Chen,Kathiravan Periasamy,David W Coltman,Meng-Hua Li,Innokentyi Ammosov,Guang-Jian Liu,Ali Esmailizadeh,Johannes A Lenstra,Maryam Nosrati,Vahideh Rezaei,Rasmus Nielsen,Xing-Long Xie,Dong-Feng Wang,Xin Li,Juha Kantanen,Diana Aguilar-Gómez,Ya-Xi Xu

doi:10.1038/s42003-021-02817-4

Abstract

The domestication and subsequent development of sheep are crucial events in the history of human civilization and the agricultural revolution. However, the impact of interspecific introgression on the genomic regions under domestication and subsequent selection remains unclear. Here, we analyze the whole genomes of domestic sheep and their wild relative species. We found introgression from wild sheep such as the snow sheep and its American relatives (bighorn and thinhorn sheep) into urial, Asiatic and European mouflons. We observed independent events of adaptive introgression from wild sheep into the Asiatic and European mouflons, as well as shared introgressed regions from both snow sheep and argali into Asiatic mouflon before or during the domestication process. We revealed European mouflons might arise through hybridization events between a now extinct sheep in Europe and feral domesticated sheep around 6000–5000 years BP. We also unveiled later introgressions from wild sheep to their sympatric domestic sheep after domestication. Several of the introgression events contain loci with candidate domestication genes (e.g., PAPPA2, NR6A1, SH3GL3, RFX3 and CAMK4), associated with morphological, immune, reproduction or production traits (wool/meat/milk). We also detected introgression events that introduced genes related to nervous response (NEURL1), neurogenesis (PRUNE2), hearing ability (USH2A), and placental viability (PAG11 and PAG3) into domestic sheep and their ancestral wild species from other wild species.

Highlights

The domestication and subsequent development of sheep are crucial events in the history of human civilization and the agricultural revolution
High-depth resequencing of 72 individuals from eight Ovis species (Fig. 1a and Supplementary Data 1) generated a total of 35.91 billion 150-bp paired-end reads (5.39 Tb), and 35.84 billion clean reads (5.28 Tb) with an average depth of 20.7× (12.2–36.9×) per individual and average genome coverage of 97.2% (96.5%–98.3%) after filtering
1.88% structural variants (SVs) were located in exonic regions, 65.2% SVs were located in intergenic regions, and 29.9% SVs were located in intronic regions, while 67.0%, 31.0%, and 0.66% SNPs were in intergenic, intronic, and exonic regions, respectively (Supplementary Tables 5 and 6)

Summary

Introduction

The domestication and subsequent development of sheep are crucial events in the history of human civilization and the agricultural revolution. We found introgression from wild sheep such as the snow sheep and its American relatives (bighorn and thinhorn sheep) into urial, Asiatic and European mouflons. We observed independent events of adaptive introgression from wild sheep into the Asiatic and European mouflons, as well as shared introgressed regions from both snow sheep and argali into Asiatic mouflon before or during the domestication process. The genus Ovis spans ~8.31 million years of evolution and comprises eight extant species: domestic sheep O. aries, argali O. ammon, Asiatic mounflon O. orientalis, European mouflon O. musimon, urial O. vignei, bighorn sheep O. canadensis, thinhorn sheep O. dalli and snow sheep O. nivicola[1]. We explored gene flow between species and selection signatures of domestication These findings added to our understanding of the origins of the Asiatic and European mouflons and the emergence of domestic sheep

Methods

Results

Conclusion