Do Interactions among Microbial Symbionts Cause Selection for Greater Pathogen Virulence?

Abstract

The ecological and evolutionary consequences of microbiome treatments aimed to protect plants and animals against infectious disease are not well understood, even as such biological control measures become more common in agriculture and medicine. Notably, we lack information on the impacts of symbionts on pathogen fitness with which to project the consequences of competition for the evolution of virulence. To address this gap, we estimated fitness consequences for a common plant pathogen, Ustilago maydis, over differing virulence levels and when the host plant (Zea mays) is co-infected with a defensive symbiont (Fusarium verticillioides), and compared these fitness estimates to those obtained when the symbiont is absent. Here, virulence is measured as the reduction in the growth of the host caused by pathogen infection. Results of aster statistical models demonstrate that the defensive symbiont most negatively affects pathogen infection and that these effects propagate through subsequent stages of disease development to cause lower pathogen fitness across all virulence levels. Moreover, the virulence level at which pathogen fitness is maximal is higher in the presence of the defensive symbiont than in its absence. Thus, as expected from theory for multiple parasites, competition from the defensive symbiont may cause selection for increased pathogen virulence. More broadly, we consider that the evolutionary impacts of interactions between pathogens and microbial symbionts will depend critically on biological context and environment, and that interactions among diverse microbial symbionts in spatially heterogenous communities contributes to the maintenance of the highly diverse symbiotic functions observed in these communities.

Tolerance-conferring defensive symbionts and the evolution of parasite virulence

“…May et al 2022). May et al (2022) have shown that when a plant host (Zea mays) is infected by a pathogenic fungus (Ustilago maydis), parasite fitness is maximised at higher levels of virulence in the presence of a defensive symbiont (Fusarium verticillioides), in agreement with our model. However, experimentally coevolved pathogenic Staphylococcus aureus and protective Enterococcus faecalis in Caenorhabditis elegans hosts, which led to a reduction in pathogen virulence; the same study system has also been shown to generate fluctuating selection dynamics in pathogen virulence and host protection (Ford et al 2017).…”

“…To date, few studies have experimentally explored the evolution of parasite virulence in the presence of defensive symbionts (King et al 2016;Ford et al 2017;G. May et al 2022).…”

“…To date, few studies have experimentally explored the evolution of parasite virulence in the presence of defensive symbionts (King et al 2016; Ford et al 2017; G. May et al 2022). May et al (2022) have shown that when a plant host ( Zea mays ) is infected by a pathogenic fungus ( Ustilago maydis ), parasite fitness is maximised at higher levels of virulence in the presence of a defensive symbiont ( Fusarium verticillioides ), in agreement with our model.…”

“…To date, few studies have experimentally explored the evolution of parasite virulence in the presence of defensive symbionts (King et al 2016; Ford et al 2017; G. May et al 2022). May et al (2022) have shown that when a plant host ( Zea mays ) is infected by a pathogenic fungus ( Ustilago maydis ), parasite fitness is maximised at higher levels of virulence in the presence of a defensive symbiont ( Fusarium verticillioides ), in agreement with our model. However, Ford et al (2016) experimentally coevolved pathogenic Staphylococcus aureus and protective Enterococcus faecalis in Caenorhabditis elegans hosts, which led to a reduction in pathogen virulence; the same study system has also been shown to generate fluctuating selection dynamics in pathogen virulence and host protection (Ford et al 2017).…”

Tolerance-conferring defensive symbionts and the evolution of parasite virulence

“…To date, few studies have experimentally explored the evolution of parasite virulence in the presence of defensive symbionts ( King et al, 2016 ; Ford et al, 2017 ; G. May et al, 2022 ). May et al (2022) have shown that when a plant host ( Zea mays ) is infected by a pathogenic fungus ( Ustilago maydis ), parasite fitness is maximized at higher levels of virulence in the presence of a defensive symbiont ( Fusarium verticillioides ), in agreement with our model.…”