Adapting to life in metal polluted rivers: implications for conservation, genetic diversity and fisheries management in the brown trout (Salmo trutta)

Abstract

During an era of unprecedented biodiversity loss, conservation ecology seeks to understand the drivers of declines, scale of impact and how to best mitigate and minimise ongoing threats to biodiversity. Within this field there is increasing awareness of the importance of understanding population genetics, as this can reveal the realised impact of stressors on diversity, how evolution responds to shape populations and their ability to adapt. Due to a long industrial history, the landscapes and ecosystems of the British Isles are amongst the most heavily influenced by anthropogenic impact in the world. This includes a once globally important mining industry which now leaves a legacy of minewater pollution which is acutely toxic to much freshwater life. Despite this, trout appear to persist within many metal impacted systems, with prior work suggesting a small number of impacted populations are genetically distinct and exhibit tolerance mechanisms to survive. In this thesis, the interactions of minewater pollution across the British Isles on the population genetics of phylogeographically divergent populations are examined. The development of a SNP assay is detailed, with this used to understand the scale of neutral genetic diversity and structure across 1,236 individuals representing 71 sampled populations from metal-impacted regions. Demographic history modelling is applied to understand the most credible scenarios to explain the observed genetic structure. I utilise newly developed low-coverage whole genome sequencing methodologies to investigate the scale of parallel adaptation, as well as examining individual adaptations within populations. Lastly, I examine the influence of minewater pollution in shaping the larger structure and diversity of the trout genome. The results demonstrate that metal-impacted trout are genetically distinct from nearby relatively non metal impacted populations, have reduced genetic diversity and these patterns are most credibly explained by recent metal-driven divergence. I demonstrate genomic regions of parallel adaptation to minewater that are more prevalent in geographically proximate populations than those with similar mixtures of metals, and novel adaptations within individual populations. We see that the genomes of individuals from impacted populations have large structural changes and high levels of transposon content, with structural variation driving functional changes in candidate genes for adaptation. These results demonstrate the ability of trout to adapt to highly stressful environments, emphasise the importance of gene flow in maintaining population viability and give insight into the mechanisms of evolution within wild populations in complex systems.