Evolution of virulence in opportunistic pathogens: generalism, plasticity, and control

Abstract

Standard virulence evolution theory assumes that virulence factors are maintained because they aid parasitic exploitation, increasing growth within and/or transmission between hosts. An increasing number of studies now demonstrate that many opportunistic pathogens (OPs) do not conform to these assumptions, with virulence factors maintained instead because of advantages in non-parasitic contexts. Here we review virulence evolution theory in the context of OPs and highlight the importance of incorporating environments outside a focal virulence site. We illustrate that virulence selection is constrained by correlations between these external and focal settings and pinpoint drivers of key environmental correlations, with a focus on generalist strategies and phenotypic plasticity. We end with a summary of key theoretical and empirical challenges to be met for a fuller understanding of OPs.

Intensive aquaculture selects for increased virulence and interference competition in bacteria

“…To conclude, in accordance with the theoretical predictions [1,[7][8][9]21], our data are consistent with the hypothesis that intensive farming conditions (high host densities, increased transmission opportunities, co-infections, possibility for serial passage, availability of nutrients, use of chemotherapy) can select for pathogen strains with the ability to produce large population sizes with high virulence that have high competitive ability under short time scales. This indicates a genetic difference in populations of high-and low-virulence bacterial strains resulting in selection for strains with an increased ability to exploit the fish host as a nutrient source.…”

“…The strains isolated from outlet water were more virulent and able to produce higher maximum population sizes than the inlet water strains, indicating that the bacteria with the best ability to exploit fish populations benefit the most in the intensive aquaculture conditions. Opportunistic lifestyle and ability to persist outside a host opens less stringent trajectories for virulence evolution, in contrast with the obligate pathogens restricted by the transmission-virulence trade-off [8], but factors that increase or limit virulence evolution in opportunistic pathogens are still poorly understood. F. columnare can be considered an opportunist, as it is known to survive long periods outside the host and transmit efficiently from dead hosts [38][39][40].…”

“…This can be especially important for environmentally transmitted opportunistic pathogens, which often have the ability to survive and replicate outside hosts. These opportunistic pathogens do not suffer from the transmission-virulence trade-off that is characteristic of obligate pathogens, which are dependent on host survival during transmission, thus significantly altering pathogen virulence [8].…”

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

“…Genotypes can have broader thermal performance range without always paying a visible performance cost at optimum conditions, but possibly involving a trade‐off with other traits (Huey & Hertz, 1984; Ketola et al., 2013), such as virulence (Ketola et al., 2013; Sturm et al., 2011). For environmentally growing opportunist pathogens, adaptations for more efficient exploitation of one growth environment could be expected to cause repercussions in their ability to grow in the other environment (Brown et al., 2012), such as host environment. Alternatively, the presence of virulence factors in the bacteria is unnecessary during the planktonic state but essential for the infection process, helping bacteria to save energy by not expressing virulence genes until they sense they have entered the host environment (Guijarro et al., 2015).…”

“…Global warming may benefit many bacterial species, because they will face milder winter months resulting in greater overwintering success, increased numbers of generations and, thus, higher pathogen densities to damage hosts (Burdon & Chilvers, 1982; Coakley, Scherm, & Chakraborty, 1999). Environmentally growing opportunistic pathogens, in contrast to obligate (fully host‐dependent) pathogens, can utilize outside‐host resources, making them very sensitive to selection pressures outside the host (Brown, Cornforth, & Mideo, 2012). Therefore, predicting the effect of climate warming on environmental opportunistic bacteria with life cycles both outside and inside the host presents a particular challenge because pathogen fitness in both environments may be differentially affected by temperature (Harvell et al., 2002).…”