Competition and facilitation between parasites as drivers of virulence evolution – EVOLVIR

Theory predicts that coinfections, when a host harbours more than one parasite, can drive epidemics and virulence evolution. Competition between parasites for shared host resources, or mediated via the immune system, are predicted to select for higher virulence. In contrast, facilitation between parasites may select for lower virulence. Thus, coinfection may have wide-reaching consequences for public health, agriculture and the basic understanding of processes shaping natural communities. Despite this, there are no empirical tests of the above predictions on parasite virulence evolution.

This project uses experimental evolution to address the interplay between coinfection driven selection in the within-host environment, and multiple infections across a population of hosts (different parasite strains or species co-circulating) for virulence evolution. It is important to consider the relationship between parasite traits in the within- and between-host environment because higher virulence favoured in a coinfected host may not be selected across the parasite population (if it cannot transmit to new hosts).

The positive and negative effects of coinfection on virulence evolution will be investigated using different parasite species (the spider mites Tetranychus urticae and T. evansi, and tomato spotted wilt virus, TSWV) infecting the tomato host (Solanum lycopersicum). T. evansi and T. urticae compete for shared host resources and interact via the host immune system; TSWV positively affects T. urticae via negative immune cross-talk and/or the release of free amino acids.

Objective 1 will investigate whether competition (between T. urticae and T. evansi) and facilitation (between T. urticae and TSWV) can drive virulence evolution in the within-host environment when parasites are constrained to be in coinfection each generation with natural transmission to new hosts. Experimental evolution will be coupled with mathematical models to address how these interactions impact virulence evolution. This will reveal whether interactions in the within-host environment are important for virulence evolution, but it is unlikely that sequential coinfection at each generation reflects epidemiological dynamics in natural populations.

Objective 2 will address this by allowing parasites to evolve in semi-natural host populations harbouring multiple infections; different parasite species co-occurring in a host population, not necessarily in the same host. Thus parasites may be in a coinfection one generation and a single infection the next. Here interactions in the within- host environment will only drive virulence evolution if there is a high frequency of coinfected hosts. Objective 2 will also identify natural tomato populations with multiple infections of T. evansi and T. urticae, and TSWV and T. urticae, to see if dynamics in the laboratory parallel epidemics in the field.

This project builds on previous studies of parasite evolution in both content and approach. Spider mite parasites are unique in that individual life-history traits can be linked to population measures of virulence. Theoretical and laboratory experiments will be employed to reveal the impact of different interaction types, and for the first time the relative importance of the within- and between-host environment, for virulence evolution in coinfections investigated. Empirical tests of theoretical predictions will provide proof of concept showing that coinfection driven parasite evolution can occur over relatively short time-scales. This approach to studying parasite evolution in individual plants, reinforced by the epidemiological component, and following evolution in laboratory and natural populations, will make headway towards a deeper understanding of the evolutionary consequences of coinfections.