Integrating reaction norm models and genome-wide association analyses to reveal the genetic architecture and environmental sensitivity of sexual precocity in Nellore cattle

Reproductive efficiency is an important component of profitability and sustainability in beef cattle production, particularly in tropical environments where animals are routinely exposed to environmental stressors. This study aimed to identify environmentally sensitive SNPs associated with sexual precocity traits in Nellore cattle and characterize candidate genes and biological pathways regulating sexual precocity under variable environmental conditions. For this purpose, three sexual precocity indicators were analyzed; one in heifers (heifer early calving probability at 30 months, HC30), and two in young males (scrotal circumference at 365 days, SC365; age at puberty, APM). Reaction norm models were integrated with genome-wide association studies (GWASs) to identify genomic regions associated with both genetic potential (intercept) and environmental sensitivity (slope). A total of 46 significant SNPs were identified across the three traits, with SC365 showing the highest genetic complexity (36 SNPs), followed by HC30 (7 SNPs), and APM (3 SNPs). The analyses revealed distinct genetic architectures among the traits. For HC30, candidate genes showed clear functional partitioning between those associated with baseline fertility (e.g., ERBB4, SNAI2) and those associated with environmental sensitivity (e.g., TRIB1, NSMCE2), with no overlap between intercept and slope components. In contrast, SC365 exhibited substantial genetic overlap, with five genes (i.e., GRB14, SLC9A8, SPATA2, MGRN1, SEPTIN12) significantly associated with both intercept and slope, indicating a robust trait with shared genetic control of baseline potential and environmental responsiveness. For APM, genetic associations were predominantly related to baseline potential, with genes involved in DNA repair (CHEK2), endoplasmic reticulum stress response (XBP1), and immune regulation (TNIP3). Functional enrichment analyses revealed trait-specific biological pathways, whereas QTL enrichment demonstrated biologically coherent overlaps with reproductive and metabolic traits. These findings demonstrate that sexual precocity traits exhibit distinct genetic architectures reflecting their underlying biological mechanisms and environmental responsiveness, providing valuable insights for developing climate-resilient breeding strategies in tropical beef cattle production systems.