Early-life conditions shape baseline immune gene expression, but not pathogen-induced immune activation, in brown trout

Early-life environment and parental background can shape immune phenotypes, but whether such differences persist during infection and influence the immune response remains unclear. We used single-cell RNA sequencing to characterize kidney immune responses in brown trout (Salmo trutta) from three origins differing in parental history and early rearing: wild parents with offspring reared in the wild; wild parents with offspring reared in a hatchery; and hatchery parents with offspring reared in a hatchery. All fish originated from the same river and showed no detectable genetic population structure. Fish were exposed to Tetracapsuloides bryosalmonae, the causative agent of proliferative kidney disease, and analyzed 25 days later alongside unexposed controls. Across 18 scRNA-seq datasets, we identified 30 cell clusters and found a clear transcriptional imprint of developmental and parental history in the resting immune system. In unexposed fish, origin was associated with pronounced differences in gene expression, particularly in B cells. When fish were subsequently exposed to the pathogen and developed subclinical infections, both immune-cell composition and transcriptional state experienced pronounced changes: T cells increased in relative abundance, while B cells, neutrophils and proliferating progenitors showed the strongest transcriptional responses, consistent with an active but controlled subclinical response. Strikingly, the strong origin-dependent differences present before exposure largely disappeared after infection. Fish from all three backgrounds converged on a shared transcriptional response, and genes associated with origin showed little overlap with those responding to infection. Thus, at single-cell resolution in vivo, we identify infection-induced transcriptional convergence across distinct environmental and parental backgrounds. Our findings show that substantial baseline immune variation can persist under resting conditions yet be overridden by pathogen exposure, constraining distinct immune states towards a common response.