Abstract
Predicting the effects of global increase in temperatures on disease virulence is challenging, especially for environmental opportunistic bacteria, because pathogen fitness may be differentially affected by temperature within and outside host environment. So far, there is very little empirical evidence on the connections between optimal temperature range and virulence in environmentally growing pathogens. Here, we explored whether the virulence of an environmentally growing opportunistic fish pathogen, Flavobacterium columnare, is malleable to evolutionary changes via correlated selection on thermal tolerance. To this end, we experimentally quantified the thermal performance curves (TPCs) for maximum biomass yield of 49 F. columnare isolates from eight different geographic locations in Finland over ten years (2003–2012). We also characterized virulence profiles of these strains in a zebra fish (Danio rerio) infection model. We show that virulence among the strains increased over the years, but thermal generalism, and in particular tolerance to higher temperatures, was negatively associated with virulence. Our data suggest that temperature has a strong effect on the pathogen genetic diversity and therefore presumably also on disease dynamics. However, the observed increase in frequency and severity of F. columnare epidemics over the last decade cannot be directly linked to bacterial evolution due to increased mean temperature, but is most likely associated with factors related to increased length of growing season, or other time‐dependent change in environment. Our study demonstrates that complex interactions between the host, the pathogen and the environment influence disease virulence of an environmentally growing opportunistic pathogen.
Highlights
Climate projections suggest that changing climate affects the average temperature and the occurrence of extreme and variable temperatures (IPCC, 2007)
We showed that Finnish isolates differed in maximum yield and limits of thermal range and that their higher tolerance to high temperatures was linked to lowered virulence
Two alternative approaches were used to analyse the thermal performance data: (a) for each strain, curve fitting using all maximum yield values followed by single-point estimation of thermal performance curves (TPCs) parameters and (b) principal component analysis (PCA) on the maximum yield values averaged per temperature for each strain
Summary
Climate projections suggest that changing climate affects the average temperature and the occurrence of extreme and variable temperatures (IPCC, 2007). Previous studies suggest that higher temperatures select genotypes that tolerate hotter temperatures, whereas fluctuations in temperature should select for more generalist genotypes with improved tolerance to extreme temperatures (Condon, Cooper, Yeaman, & Angilletta, 2014; Condon et al, 2015; Duncan, Fellous, Quillery, & Kaltz, 2011; Kassen, 2002; Ketola et al, 2013; Levins, 1968) It has remained unclear how climate warming might affect growth parameters in environmentally growing opportunistic pathogens, and how this correlates with their potential to cause disease. We showed that Finnish isolates differed in maximum yield and limits of thermal range and that their higher tolerance to high temperatures was linked to lowered virulence
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