@article{02a97ddd506a49ae91ec0e980a5fb5c1,
title = "The Genomic Signature and Transcriptional Response of Metal Tolerance in Brown Trout Inhabiting Metal-Polluted Rivers",
abstract = "Industrial pollution is a major driver of ecosystem degradation, but it can also act as a driver of contemporary evolution. As a result of intense mining activity during the Industrial Revolution, several rivers across the southwest of 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 analysis of six populations (originating from three metal-impacted and three control rivers) revealed strong genetic substructuring between impacted and control populations. We identified selection signatures at 122 loci, including genes related to metal homeostasis and oxidative stress. Trout sampled from metal-impacted rivers exhibited significantly higher tissue concentrations of cadmium, copper, nickel and zinc, which remained elevated after 11 days in metal-free water. After depuration, we used RNAseq to quantify gene expression differences between metal-impacted and control trout, identifying 2042 differentially expressed genes (DEGs) in the gill, and 311 DEGs in the liver. Transcriptomic signatures in the gill were enriched for genes involved in ion transport processes, metal homeostasis, oxidative stress, hypoxia, and response to xenobiotics. Our findings reveal shared genomic and transcriptomic pathways involved in detoxification, oxidative stress responses and ion regulation. Overall, our results demonstrate the diverse effects of metal pollution in shaping both neutral and adaptive genetic variation, whilst also highlighting the potential role of constitutive gene expression in promoting metal tolerance.",
keywords = "RADseq, RNAseq, adaptation, freshwater, pollution, toxic metals",
author = "Paris, {Josephine R.} and King, {R. Andrew} and {Ferrer Obiol}, Joan and Sophie Shaw and Anke Lange and Vincent Bourret and Hamilton, {Patrick B.} and Darren Rowe and Laing, {Lauren V.} and Audrey Farbos and Karen Moore and Urbina, {Mauricio A.} and {van Aerle}, Ronny and Catchen, {Julian M.} and Wilson, {Rod W.} and Bury, {Nicolas R.} and Santos, {Eduarda M.} and Stevens, {Jamie R.}",
note = "Funding: This work was supported by Westcountry Rivers Trust, UK, Charity No. 1135007, Company No. 06545646; University of Exeter; Biotechnology and Biological Sciences Research Council, BB/K003240/1; Environment Agency, UK; Wellcome Trust, WT097835MF, WT101650MA. The authors wish to dedicate this article to Professor Mike Bruford, who was the external viva voce examiner of the PhD thesis of JRP, and who offered valuable advice on the research. Environmental data were provided by the Environment Agency Devon and Cornwall Teams. Fieldwork, electrofishing, permits and access to sites were planned and undertaken with assistance from the Westcountry Rivers Trust, in particular Matthew Healey and Giles Rickard. Fieldwork was assisted by Janice Shears, Philip Shears and Adam Porter. The UK Environment Agency provided assistance in the collection of water chemistry features and selection of appropriate sampling sites. Simon Toms (UK Environment Agency) granted permission to collect wild brown trout for the physiology experiment. Aquatic Research Centre (ARC) staff at the University of Exeter provided assistance with fish husbandry and experimental design, in particular Gregory Paull and Charles Tyler who oversaw the ethical aspects of the laboratory experiment and who provided guidelines on Home Office Regulations. Jennifer Fitzgerald, Rebecca Millard and Hannah Littler assisted with experimental sampling. RAD-seq and RNA-seq sequencing was performed at the University of Exeter Sequencing Service, which utilised equipment funded by the Wellcome Trust Institutional Strategic Support Fund (WT097835MF), Wellcome Trust Multi-user Equipment Award (WT101650MA) and BBSRC LOLA award (BB/K003240/1). Research was co-funded by the Environment Agency, the Westcountry Rivers Trust, and the University of Exeter. For the purpose of open access, the author has applied a Creative Commons Attribution (CC BY) licence to any Author Accepted Manuscript version arising from this submission. This work was supported by Westcountry Rivers Trust, UK, Charity No. 1135007, Company No. 06545646; University of Exeter; Biotechnology and Biological Sciences Research Council, BB/K003240/1; Environment Agency, UK; Wellcome Trust, WT097835MF, WT101650MA. Funding: The authors wish to dedicate this article to Professor Mike Bruford, who was the external viva voce examiner of the PhD thesis of JRP, and who offered valuable advice on the research. Environmental data were provided by the Environment Agency Devon and Cornwall Teams. Fieldwork, electrofishing, permits and access to sites were planned and undertaken with assistance from the Westcountry Rivers Trust, in particular Matthew Healey and Giles Rickard. Fieldwork was assisted by Janice Shears, Philip Shears and Adam Porter. The UK Environment Agency provided assistance in the collection of water chemistry features and selection of appropriate sampling sites. Simon Toms (UK Environment Agency) granted permission to collect wild brown trout for the physiology experiment. Aquatic Research Centre (ARC) staff at the University of Exeter provided assistance with fish husbandry and experimental design, in particular Gregory Paull and Charles Tyler who oversaw the ethical aspects of the laboratory experiment and who provided guidelines on Home Office Regulations. Jennifer Fitzgerald, Rebecca Millard and Hannah Littler assisted with experimental sampling. RAD\u2010seq and RNA\u2010seq sequencing was performed at the University of Exeter Sequencing Service, which utilised equipment funded by the Wellcome Trust Institutional Strategic Support Fund (WT097835MF), Wellcome Trust Multi\u2010user Equipment Award (WT101650MA) and BBSRC LOLA award (BB/K003240/1). Research was co\u2010funded by the Environment Agency, the Westcountry Rivers Trust, and the University of Exeter. For the purpose of open access, the author has applied a Creative Commons Attribution (CC BY) licence to any Author Accepted Manuscript version arising from this submission.",
year = "2025",
month = jan,
doi = "10.1111/mec.17591",
language = "English (US)",
volume = "34",
journal = "Molecular ecology",
issn = "0962-1083",
publisher = "Wiley-Blackwell",
number = "1",
}