Single-cell analysis of a salmonid immune system (river brown trout Salmo trutta fario) reveals evolutionary divergence and hatchery-induced transcriptional reprogramming.

Abstract

<h4>Background</h4>Vertebrate immune systems exhibit striking evolutionary diversity, yet our understanding remains biased toward mammalian models. Here, we generate a single-cell transcriptome of immune cells from the ecologically and economically important salmonid Salmo trutta fario (river brown trout), a lineage characterized by an ancestral whole-genome duplication (WGD).<h4>Results</h4>Profiling over 83,000 kidney-derived immune cells, we resolved 34 transcriptionally distinct populations, identified core immune lineages, and uncovered novel markers in neutrophils, macrophages, T-cells, and B-cells. We detected pervasive transcriptional divergence between WGD-derived ohnologue pairs, indicating putative sub- and neofunctionalization in immune gene regulation. We further show that the transcriptional identity of immune cells is shaped by rearing history: fish raised in hatcheries-whether for one or multiple generations-showed shifts in immune gene expression across cell types.<h4>Conclusions</h4>Our findings provide baseline data for the healthy brown trout cellular immune system, insight into the evolution of vertebrate immunity, and avenues for understanding the molecular basis of reduced immunological fitness of hatchery-reared fish.