Runs of homozygosity reveal population dynamics and selection across global cattle

Cattle have undergone complex evolutionary trajectories shaped by domestication, migration, and selection. Although runs of homozygosity (ROH) are a ubiquitous genomic feature, their full potential to decipher the evolutionary history and functional consequences in global cattle populations remains underexplored. We analyzed whole-genome sequences from 102 breeds across 17 geographic regions to conduct a global investigation of ROH landscapes, population structure, genomic inbreeding, and functional variants.

ROH patterns revealed elevated homozygosity burdens in intensively selected European breeds, whereas South Chinese indicine showed a high short ROH burden, suggestive of a unique ancient demography. ROH-based principal component analysis (PCA) and admixture delineated taurine-indicine lineages, region-specific ancestries, inbreeding, and breeding effects. ROH-based inbreeding coefficient (F_ROH) exhibited greater stability for cross-population inbreeding assessment, showing a high correlation with excess of homozygosity-based inbreeding coefficient (F_HOM) and a negative association with heterozygosity. Region-specific ROH hotspots, identified via permutation test, reflected a combination of local adaptation and demographic legacies. Trait-focused analyses, cross-validated with multiple selection scans, identified genes underlying growth, milk, and climate adaptation. Notably, we found missense mutations in CHEK2, SPG7, FANCA, and MSRB3, whose frequencies were significantly correlated with temperature and humidity.

This study establishes ROH as a pivotal genomic marker for illuminating the dynamics of domestication, migration, inbreeding, and selection. Our findings offer valuable resources and insights for advancing genetic conservation and precision breeding in cattle under the pressures of climate change.