Maternal reproductive precocity shapes immunometabolic responses to lipopolysaccharide challenge in Japanese quail offspring.

Productive efficiency in laying breeders is influenced by genetic and physiological factors, but it remains unclear whether maternal reproductive precocity programs distinct inflammatory responses in the offspring. This study evaluated the effects of maternal precocity on productive performance, immunological parameters, and the intestinal transcriptomic profile of Japanese quail offspring challenged with lipopolysaccharide (LPS). A design with two maternal groups was used (early-maturing: reaching 95% lay between weeks 14-15; and late-maturing: between weeks 17-18), and the offspring were either challenged or not with LPS at 25 days of age, with jejunum collection for RNA sequencing. Early-maturing dams showed better productive performance and lower stress indicators (lower heterophil:lymphocyte ratio and lower relative spleen weight) (p < 0.05). Their offspring, when challenged with LPS, exhibited a metabolic suppression profile, with downregulation of genes linked to oxidative phosphorylation (NDUFA5, NDUFS6; adj. p = 0.006 for the oxidative phosphorylation pathway), NADH metabolism (GPD1; adj. p = 0.005 for NADH metabolic process), and amino acid transport (SLC25A13, SLC25A15; adj. p = 0.005 for l-amino acid transmembrane transport), associated with activation of anti-inflammatory mediators (IL18BP, IL1R2; adj. p = 0.032 for cytokine binding), characterizing an energy-saving tolerance strategy to inflammation. In contrast, the offspring of late-maturing dams challenged with LPS showed strong activation of matrix metalloproteinase MMP7 (adj. p = 0.004 for collagen catabolic process) and exclusive enrichment of the Wnt signaling pathway (adj. p = 0.003), indicating a response directed toward extracellular matrix remodeling and tissue repair. In conclusion, maternal precocity programs two distinct transcriptional phenotypes in the offspring facing an inflammatory challenge: metabolic tolerance with immunomodulation (descendants of early-maturing dams) versus resistance with tissue remodeling (descendants of late-maturing dams), demonstrating that maternal genetic merit determines different resource allocation strategies between immune defense and homeostasis maintenance.