Developmental dynamics of crop morphology, microbiota, and mucosal immunity in chickens.

BACKGROUND: The crop is a unique anterior digestive organ in poultry that functions in temporary feed storage and lactic acid bacteria-dominated fermentation, thereby interacting with the gastrointestinal tract to influence gut health and feed efficiency. However, its developmental characteristics and functional establishment across the entire growth cycle remain poorly understood. RESULTS: A slow-growing chicken breed (Lueyang Black-boned chicken) was used to characterize dynamic changes in crop histomorphology, mucosal immune status, and microbiota from hatch to adulthood (d 1, 14, 28, 42, 56, 70, 98, and 140; n = 10 per time point). Crop development was divided into two stages. From d 1 to d 42, the crop underwent structural and microbial establishment. This stage was characterized by a slow increase in crop weight, progressive thickening and stabilization of the muscular and mucosal layers, and a gradual increase in secretory immunoglobulin A (sIgA) levels. Genes involved in mucin synthesis and modification were markedly upregulated during early development (d 1 to d 14). Meanwhile, the microbiota shifted from environmentally associated facultative anaerobes to lactic acid bacteria-dominated communities (Lactobacillus, Ligilactobacillus, and unclassified Bacilli). Correspondingly, predicted microbial functions shifted from colonization-related pathways to carbohydrate, fatty acid, and butyrate metabolism. From d 42 to d 140, the crop entered a stage of structural expansion and microbial restructuring. Crop weight increased rapidly, and the mucosal layer exhibited fluctuations, while sIgA levels continued to increase and stabilized. During d 42 to d 56, fluctuations in mucosal thickness were accompanied by reduced mucin sialylation. At the same time, lactic acid bacteria populations shifted, with a decrease in Ligilactobacillus and an increase in unclassified Bacilli, followed by stabilization of the microbial community. Functional prediction indicated enrichment of membrane transport systems and diverse nutrient metabolism pathways. CONCLUSION: This study demonstrates that the early post-hatch period establishes the crop's basic functions, whereas the growing period is characterized by crop expansion and further maturation of the microbial community. These findings provide a theoretical basis for targeted interventions in the crop to improve poultry production performance.