Intensive fish farming and the evolution of pathogen virulence: the case of columnaris disease in Finland

Abstract

Ecological changes affect pathogen epidemiology and evolution and may trigger the emergence of novel diseases. Aquaculture radically alters the ecology of fish and their pathogens. Here we show an increase in the occurrence of the bacterial fish disease Flavobacterium columnare in salmon fingerlings at a fish farm in northern Finland over 23 years. We hypothesize that this emergence was owing to evolutionary changes in bacterial virulence. We base this argument on several observations. First, the emergence was associated with increased severity of symptoms. Second, F. columnare strains vary in virulence, with more lethal strains inducing more severe symptoms prior to death. Third, more virulent strains have greater infectivity, higher tissue-degrading capacity and higher growth rates. Fourth, pathogen strains co-occur, so that strains compete. Fifth, F. columnare can transmit efficiently from dead fish, and maintain infectivity in sterilized water for months, strongly reducing the fitness cost of host death likely experienced by the pathogen in nature. Moreover, this saprophytic infectiousness means that chemotherapy strongly select for strains that rapidly kill their hosts: dead fish remain infectious; treated fish do not. Finally, high stocking densities of homogeneous subsets of fish greatly enhance transmission opportunities. We suggest that fish farms provide an environment that promotes the circulation of more virulent strains of F. columnare. This effect is intensified by the recent increases in summer water temperature. More generally, we predict that intensive fish farming will lead to the evolution of more virulent pathogens.

Intensive aquaculture selects for increased virulence and interference competition in bacteria

“…Since the mid-1990s F. columnare outbreak frequency, severity of symptoms and disease-related mortality have significantly increased in aquaculture, and the evolution of virulence has been suggested as an explanation [23]. Our study finds Table 3.…”

“…One contributing factor is the warming climate, which causes changes in disease ecology, outbreak dynamics and seasonality [51][52][53]. Owing to global warming, the longer outbreak period for columnaris disease [23] increases bacterium-host and bacterium-bacterium interactions, allowing greater opportunities for evolution of both virulence and competitive ability.…”

“…Information on the diseases threatening crop, livestock and aquaculture production is essential for securing world food production. Here, we study how selection in intensive aquaculture influences the virulence and the competitive ability, at both long and short time scales, in the globally significant fish pathogen Flavobacterium columnare (Bacteroidetes) [23,24]. First, we explore temporal changes in virulence and competitive ability using F. columnare strains isolated from disease outbreaks in [2003][2004][2005][2006][2007][2008][2009][2010].…”

Broad thermal tolerance is negatively correlated with virulence in an opportunistic bacterial pathogen

“…The temperature range in which it can grow actively is approximately 15 to 35°C (Declercq et al., 2013). Previous work on this bacterium and a number of other virulent pathogens in the context of global warming has focused mainly on long‐term empirical data examining the relationship between mean ambient temperature and disease prevalence (Karvonen, Rintamäki, Jokela, & Valtonen, 2010; Pulkkinen et al., 2010). As both open and flow‐through aquaculture systems are connected to natural water bodies, it can be expected that changes in ambient water temperatures strongly affect farming conditions.…”

“…Analysis of more than 20 years’ worth of data has showed a significant positive effect of mean water temperature on the prevalence of columnaris disease at two fish farms (Karvonen et al., 2010). At the same time, the data point to an increase in virulence of this bacterium in fish farms over the years (Pulkkinen et al., 2010), which might have happened due to selection for certain genotypes of the bacterium (Sundberg et al., 2016). However, it is still unclear whether climate change will impact the thermal performance of this bacterium in the long term by selecting more thermotolerant strains and whether such changes may have any effect on bacterial virulence.…”