Precision livestock farming and integrated molecular profiling reveal heat-stress resilience signatures in Marchigiana cattle.

Introduction: Heat stress is an increasing challenge for cattle welfare and biological efficiency under climate change. Locally adapted and less intensively selected breeds may represent models for investigating resilience mechanisms, as they may retain adaptive traits useful for the selection of heat-resilient animals. This study characterized the response of Marchigiana cattle, a local Italian beef breed adapted to semi-extensive environments, in comparison with two cosmopolitan breeds with different productive aptitudes, Limousine and Holstein. Precision Livestock Farming, hematological profiling, and blood transcriptomics were integrated to investigate population- and breed-associated responses to heat stress (HS) under the specific farming conditions examined. Methods: IoT collars were applied only to Marchigiana cattle to record activity patterns and animal-proximal environmental variables. Blood samples from the three cattle populations were collected during summer HS and thermoneutral conditions, with sampling days selected according to the temperature-humidity index (THI). Results: Sensor-derived data in Marchigiana cattle identified distinct clusters with differences in movement intensity and animal-proximal THI dynamics during HS. Hematological analyses revealed population-specific responses: Holstein showed increased neutrophils and platelets, consistent with a stronger inflammatory profile, whereas Marchigiana exhibited higher red blood cell counts and hemoglobin under HS, suggesting better maintenance of systemic homeostasis. Transcriptomic analysis identified both shared and population-specific responses to HS. Although all populations activated core immune- and stress-related pathways, the magnitude and organization of the response differed markedly. Holstein displayed the broadest inflammatory, immunometabolic, and tissue-remodeling signature, Limousine showed an intermediate profile, whereas Marchigiana exhibited a more coordinated response characterized by immune modulation, redox protection, metabolic buffering, and less pronounced extracellular matrix remodeling. We performed expression quantitative trait loci (eQTL) mapping using gene expression data and whole-genome imputed or non-imputed genotypes. Using imputed or non-imputed genotypes, we identified 43 and 65 cis-eQTLs influencing the expression of 45 and 73 genes, respectively. Discussion: Our findings indicate that Marchigiana cattle exhibited hematological and transcriptomic profiles consistent with a potentially more balanced adaptive response to HS under the investigated conditions. However, because each breed was sampled on a different farm and direct physiological or productive measures of resilience were not included, the results do not establish an exclusively genetic breed effect or definitively demonstrate superior resilience. Integrating sensor-derived phenotypes with blood-based biomarkers may nevertheless help identify biological signatures associated with inter-individual responses. In addition, integrating transcriptomics and genomics identified cis-eQTLs that provide candidate regulatory markers for future studies of heat adaptation.