Environmental factors impacting Saprolegnia infections in wild fish stocks

Fish provide a primary source of protein for the rapidly expanding human population, and so it is imperative to both improve aquaculture production and protect wild fish stocks. Disease presents a major obstacle to this goal. Oomycetes of the genus Saprolegnia are endemic parasites of freshwater ecosystems that are responsible for staggering economic losses within aquaculture and have also been increasingly associated with wild salmonid declines across England and Wales. All 49 English rivers have previously experienced saprolegniasis, and moreover between 2010 and 2018, 11 of these experienced major epidemics (Chapter 2). These disease issues have exposed fundamental gaps in our knowledge of Saprolegnia epidemiology and the environmental risk factors associated with outbreaks. For the first time, this thesis employed a landscape genomics approach to study the molecular epidemiology of Saprolegnia parasitica isolates collected from wild fish hosts across England and Wales (Chapter 3). All 46 isolates examined were genetically distinct and could be separated into two subpopulations. Adaptive genomic signatures of selection were detected within gene groups that likely underpin S. parasitica pathogenesis, including those that function in: sensing external stimuli, host invasion/colonisation, infective life stages and nutrient acquisition. Furthermore, genomic adaptation was linked with environmental temperatures. The true extent of S. parasitica generalism was also investigated here (Chapter 4); among the four S. parasitica isolates examined, there was evidence of local host adaptation. An isolate displayed a preference for sea trout during in vitro induced zoospore encystment assays and also caused more sea trout than salmon mortalities in the first 48h of an experimental challenge infection. The influence of the abiotic factors, temperature and water flow, on Saprolegnia epidemics within English rivers and biological processes that contribute to transmission were assessed in Chapter 5. Records of disease outbreaks in 3 major English rivers between 2010 and 2018 could be linked with mean spring flow rates; lower flow rates in particular were found in years with increased levels of Saprolegnia. Water movement was also found to stimulate S. parasitica sporulation in a temperature dependent manner and low flows increased salmon (Salmo salar) susceptibility to saprolegniasis. Moreover, increased temperatures were found to generally increase Saprolegnia spp. vegetative growth rates and decrease S. parasitica zoospore viability. Lastly, this thesis examined the individual and combined effects of S. parasitica and various thermal regimes on the mortality of brown trout (Salmo trutta) alevins and fry (Chapter 6). Fish mortality only increased when warmer water temperatures and subsequent rapid temperature increases representative of a combination of climate change and thermopeaking were experienced at the time of S. parasitica exposure. While future work is needed to predict the potential impact of climate change on this parasite, collectively, these results improve our understanding of S. parasitica adaptation to external pressures and provide insight into disease outbreaks. This data will ultimately aid the reduction of Saprolegnia infections in aquaculture and improve the protection of wild fish populations