Living in a post-industrial landscape: repeated patterns of genetic divergence in brown trout Salmo trutta across the British Isles

Abstract

Aim: The British Isles have been worked for millennia to extract metal ores to feed industrial development, leaving a legacy of mine water pollution that continues to impact freshwater communities in many regions. Brown trout (Salmo trutta L.) have long been observed to persist in these metal-impacted systems as apex predators, with previous studies showing a small number of impacted populations to be highly genetically divergent. We sought to understand the scale of genetic diversity across regions and the repeatability of genetic divergence in trout populations affected by metal pollution. Location: We examined four mine water-impacted regions across the British Isles: west Wales, northeast England, southwest England and southeast Ireland. Methods: We employed a panel of 95 SNP loci to screen 1236 individuals from 71 sites representing paired metal-impacted and clean sites from across the four regions. From these, we obtained diversity statistics, assessed genetic structuring of populations and modelled historical demographic scenarios to understand which factors most credibly explain genetic variation in divergent populations. Results: We evidenced hierarchical population structure in the regions studied, in line with expectations from phylogeographic history. However, in a hierarchical analysis of genetic structuring the first level of differentiation was driven by the divergence of the metal-impacted trout of Cornwall in southwest England. Within regions we observed reduced genetic diversity and repeated patterns of local genetic sub-structuring between paired samples from metal-impacted and relatively clean sites. Demographic history analyses suggested the timing of these splits to be relatively recent and to be associated with periods of peak mining activity. Main conclusions: Our findings demonstrate distinct patterns of genetic isolation and reduced diversity arising from legacy pollution in freshwater ecosystems, with impacts being most apparent where both chemical pollution and physical barriers are present. Management should focus on the amelioration of mine water wash-out and the removal of barriers to fish movement to safeguard genetic diversity in impacted populations.