From molecules to populations: the genomic legacy of historic pollution on freshwater fish

Overview

Anthropogenic pollution is a critical global challenge to biodiversity. Toxic compounds from mining, manufacturing, domestic development, and industry have contaminated habitats worldwide, causing morbidity and mortality in animals. The UK was once one of the world’s industrial powerhouses. An unfortunate legacy of this success is a landscape of hot-spot high pollution sites. This studentship project will examine the effect of that pollution on native biodiversity.

Contaminants have organismal effects across scales: from nucleotides in the genome, to individual fitness, to the demography of populations. These effects can be proximate, such as DNA methylation altering gene expression, morphological development, and behaviour. The effects can also be evolutionary, via molecular adaptation to contaminants that enables organisms to persist in polluted environments. The genomic effect of complex environmental contamination in natural vertebrate populations is currently a major knowledge gap.

Understanding the complex and dynamic interplay between genetics, epigenetics, and environment is tremendously important for predicting, diagnosing, and remedying the effects of pollution on wildlife. Native brown trout (Salmo trutta) is the most widespread freshwater fish In the British Isles and is of exceptional economic importance. Brown trout is therefore a sentinel of environmental quality for riverbeds, sediments, and water (Fig. 1) and, coupled with advances in genomic resources for this species, a powerful biological model for this research.

This multidisciplinary project will advance the field by identifying the genomic and epigenomic effects of point-source and diffuse heavy metal and urban run-off pollution on native trout using a combination of natural population, molecular, and experimental approaches. Specifically, it will ask
• Does pollution affect population demography in natural ecosystems?
• Is there evidence for genomic adaptation and tolerance to pollution?
• What are the epigenomic effects of pollution on natural populations of fishes, from the scale of genome through to individual?
• Are genomic and epigenomic patterns predictable across polluted sites?

The diverse River Clyde catchment in central Scotland has a long history of extractive industry and dense human habitation. The concomitant enduring industrial legacy across the Clyde system, provides continua of pristine through highly polluted sites, and this will be the primary research and experimental area. The project will further compare with brown trout populations and genome-level effects of pollution from other contaminated sites in the UK.

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Image Captions

used with permission from W. Yeomans.

Methodology

This multidisciplinary project will integrate biological and chemical fieldwork, molecular lab work, cutting-edge and high resolution genomic, epigenomic and transcriptomic analyses, experimental manipulations, and chemical analyses. The student will receive advanced training and also have input into experimental design, analysis and research approach in this exciting new area of ecotoxicogenomics. Given the timely and urgent nature of this sort of research for environmental management and policy, we predict that the research will have high impact. The outputs will be multiple high profile publications in top journals for the fields of biology, evolution and environment.

Fieldwork: Environmental and biological samples will be collected from representative sites. Fieldwork is with CASE partner Clyde River Foundation (CRF), which has monitored the biota of the Clyde system since 2002 and has data on biotic communities across the 6,000km of watercourses. The student will be trained in electrofishing and environmental sampling. CRF will support fieldwork with a fully trained team and all necessary equipment (Fig. 2).

Contaminant analysis: Contemporary pollution levels will be investigated using standard sampling and analytical approaches for surface waters and, where appropriate for the system investigated, sediments. Contaminant concentrations will also be measured in fish tissues to provide direct measures of uptake. For metals, measurements of general water composition (pH, major ions, dissolved organic carbon) will be made in order to compute measures of metal exposure/bioavailability at impacted sites (Stockdale et al., 2010). Where available (e.g. SEPA water quality records; CRF unpublished information) historic contamination data will be sourced for sampling sites to build a picture of contamination history. The student will be trained and conduct contaminants research with co-I Lofts at CEH.

Evolutionary analysis: Population structure and demography will be inferred from high density genome-wide markers mapped to an annotated reference genome. Contemporary structure will be contextualised with demographic and landscape genomics analyses. Historical changes will be inferred from coalescent modelling. Molecular adaptation will be analysed by advanced genome-wide association and machine-learning approaches for selection.

Epigenomic analysis: The effect of pollution on the genome via DNA methylation will be assessed via tissue-specific, genome-wide molecular analyses. Leveraging these new data, bioinformatic approaches will be used to identify susceptible regions, which genes are affected and how they are affected.

Experimental approach: To validate the effect of contamination on DNA methylation, gene expression, and fish development, brown trout will be reared under experimental conditions exposed to variable levels of contaminants, recreating levels assessed in the environment. Epigenomic, gene expression, and developmental assays will be analysed in replicated time series and compared to natural population effects.

Project Timeline

Year 1

Field collections; genomic/ epigenomic data generation; environmental chemical analyses.

Year 2

Field collections; epigenomic data analysis; experimental manipulations and tests; environmental chemical analyses.

Year 3

Evolutionary and genomic analyses; molecular analyses of experimental validations.

Year 3.5

Synthesizing data analyses; Results dissemination through manuscripts and conference presentations

Training
& Skills

The student will train with internationally esteemed researchers. PI Elmer is expert in adaptation and ecological ‘omics of natural populations, including fishes. Co-I Yeomans is expert in fish health and environmental monitoring. Co-I Lofts is expert in bioavailability and toxicity of metal contaminants in the natural environment. The CASE partner, Clyde River Foundation, runs long-term monitoring of fish and environmental health at more than 1000 field sites. The student will be trained in freshwater biology field and lab skills (fish and invertebrate sampling and identification) and encouraged to become involved with the extensive CRF public engagement programme. The project will be based in Glasgow, where the student will join a successful, active, and vibrant research community at an institution of high national and international standing. The university provides high level training in core research, communication and transferable skills that bolster students for success in academia, government, or business. The data analysis and communication skills gained in this project will have key relevance for employability in conservation, aquaculture, academia, or government research.

References & further reading

Elmer KR, Fan S, Kusche H, Spreitzer M-L, Kautt AF, Franchini P, Meyer A (2014) Parallel evolution of Nicaraguan crater lake cichlid fishes by non-parallel routes. Nature Communications, 5, 6168.

Jacobs A, Hughes MR, Robinson PC, Adams CE, Elmer KR (2018) The genetic architecture underlying the evolution of a rare piscivorous life history form in brown trout after secondary contact and strong introgression. Genes, 9, 280.

Moore I, McGillivray C, Yeomans WE, Murphy K (2017) Quantifying 250 years of change to the channel structure of the River Kelvin. Glasgow Naturalist 26, 65.

O’Grady KT (1981) The recovery of the river Twymyn from lead mine pollution and the zinc loading of the recolonising fauna. Minerals and the Environment, 3, 126-137.

Reid NM, Proestou DA, Clark BW, Warren WC, Colbourne JK, Shaw JR, Karchner SI, Hahn ME, Nacci D, Oleksiak MF, Crawford DL, Whitehead A (2016) The genomic landscape of rapid repeated evolutionary adaptation to toxic pollution in wild fish. Science, 354, 1305-1308.

Stockdale A, Tipping E, Lofts S, Ormerod SJ, Clements WH, Blust R. (2010) Toxicity of proton-metal mixtures in the field: Linking stream macroinvertebrate species diversity to chemical speciation and bioavailability. Aquat Toxicol, 100, 112-119.

Yauk C, Polyzos A, Rowan-Carroll A, Somers CM, Godschalk RW, Van Schooten FJ, Berndt ML, Pogribny IP, Koturbash I, Williams A, Douglas GR, Kovalchuk O (2008) Germ-line mutations, DNA damage, and global hypermethylation in mice exposed to particulate air pollution in an urban/industrial location. Proc Natl Acad Sci U S A, 105, 605-610.

Further Information

Applications: to apply for this PhD please use the url: https://www.gla.ac.uk/study/applyonline/?CAREER=PGR&PLAN_CODES=CF18-7316

For questions please contact Dr. Kathryn Elmer, Kathryn.Elmer@glasgow.ac.uk or +44 141 330 6617

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