Abstract
BACKGROUND: Sheep have diversified into distinct breeds worldwide through both natural adaptation and human-driven selection, with hybridization serving as an effective strategy for rapid trait improvement. The Tianhua mutton sheep (TMS) is a novel breed derived from crossing South African Mutton Merino (SAMM) with Gansu alpine fine-wool sheep (GAFS). After nearly two decades of selective breeding, TMS has developed great meat quality traits and impressive cold tolerance at high altitudes. To study the genetic mechanism and provide new insights into phenotypic variation, we analyzed the genetic diversity, population structure, and selective signatures of TMS based on whole-genome sequencing of 55 TMS, 11 SAMM, and 197 public sheep genomes worldwide. RESULTS: Population genetic analysis revealed that TMS forms a distinct branch, with a pedigree composition showing an approximate 5:3 ratio of SAMM to GAFS lineages, consistent with the breeding design. Genetic diversity assessment showed that TMS exhibits higher genetic diversity and a lower inbreeding coefficient than commercial sheep from Africa, the Americas, and Europe, suggesting that TMS has considerable breeding potential to be tapped. Genome-wide scanning using the F(ST) and XP-EHH methods was also performed to detect the signatures of selection in TMS, with significance thresholds set at Z(F(ST)) >2.57 and XP-EHH >2.31. Functional annotation analysis revealed that the selected genes were related to meat quality traits, high-altitude adaptation, and disease resistance. Specifically, genes such as PLA2G10, SAMD12, CKMT2, ACOT12, and TNS3 are implicated in the processes related to fat metabolism. ZNF280D, RANBP3L, CSRP1, TNNI1, and AGBL4 are related to muscle growth and development. ABCB1 regulates energy metabolism via ATP transport to enhances low-oxygen adaptation, while NOTCH3, FBXO32, and LAMA1 regulate cardiopulmonary function and reduce pulmonary hypertension. Additionally, ATM, GALNTL6, and B4GALT5 may improve disease resistance and enhance environmental adaptability. CONCLUSION: The results provide valuable insights for investigating the genetic mechanisms underlying TMS fine traits, enhancing TMS breeding, and developing mutton sheep suited to high-altitude and cold environments. Furthermore, it also indicates that hybrid breeding represents an effective strategy to provide a source of phenotypic variation for local adaptation and rapid acquisition of agronomically important traits.