Combining population genomics and transcriptomics to identify signatures of metal tolerance in brown trout inhabiting metal-polluted rivers

Industrial pollution is a major factor responsible for the degradation of ecosystems but can also act as a driver of contemporary evolution. As a result of intense mining activity during the Industrial Revolution, several rivers across southwest England are polluted with high concentrations of metals. Despite the documented negative impacts of ongoing metal pollution, brown trout ( Salmo trutta L.) survive and thrive in many of these metal-impacted rivers. We used population genomics, transcriptomics, and metal burdens to investigate the genomic and transcriptomic signatures of potential metal tolerance. RADseq of six populations (originating from three metal-impacted and three control rivers), identified strong genetic substructuring between metal-impacted populations, and selection signatures at 122 loci, including genes involved in metal homeostasis and oxidative stress. Measuring the tissue-metal burden (cadmium, copper, nickel, zinc) in metal-impacted and control trout populations, we identified significantly higher metals in metal-impacted trout sampled from the river, and after 11 days of depuration in control water. After depuration, we used RNAseq to quantify gene expression differences between metal-impacted and control trout, identifying 2,042 differentially expressed genes (DEGs) in the gill, and 311 DEGs in the liver. Transcriptomic signatures in the liver were nuanced, but in the gill, ion transport processes were enriched, alongside the over-expression of genes involved in metal homeostasis, and response to oxidative stress, hypoxia and xenobiotics. Our results demonstrate the complexity of metal tolerance in vertebrates and offer insights into the potential adaptive processes underpinning evolution to pollution in teleost fish. ### Competing Interest Statement The authors have declared no competing interest.