Sub-lethal effects of pathogens can lead to the evolution of lower virulence in multiple infections

Schjørring, S., & Koella, J. C. (2003). Sub-lethal effects of pathogens can lead to the evolution of lower virulence in multiple infections. Proceedings of the Royal Society of London B: Biological Sciences, 270(1511), 189-193.

Multiple infections are common in nature, but the impact of co-infection relative to single infection on parasite virulence is not consistent. Theory suggests that multiple infections will lead to higher parasite virulence because competition within hosts means that the most successful parasites will be those that exploit the host fastest (i.e. have higher virulence), but experimental studies often find contradictory patterns. These varying relationships between co-infection and virulence could stem from tradeoffs between competitive ability and growth rate of parasites, or from cooperation between parasites; cooperation would lead to decreased virulence because parasite fitness would increase with the time of co-infection, which would de-incentivize high virulence. In addition, one main assumption of the theory of increasing virulence with multiple infections is that parasites decrease a host’s lifespan. However, many parasites have sublethal effects (e.g. on growth), and thus may not benefit from exploiting their host too quickly, especially if their growth rates are determined by the size or quality of their host. In this paper, Schjørring and Koella (2002) use a theoretical model to explore optimal parasite virulence when parasites have either lethal or sublethal effects on their host.

The model the authors create is based on macroparasites, though it could be generalized to microparasites as well. Infection intensity is fixed, and the number of individuals of each parasite genotype within a host is determined by their abundance in the parasite population overall. They model feedbacks between host growth, which is determined by parasite growth effect and constrained by a maximum size, and parasite growth, which is determined by the size of the host and the parasite’s growth effort. One parameter (a) controls the relationship between parasite growth and host mortality, and another (b) controls the relationship between parasite growth and host growth. By contrasting the two extremes of these parameter values (a=0, b=1 and a=1, b=0), Schjørring and Koella can determine the optimal virulence (i.e. parasite growth effort) for parasites in single and multiple infections.

When exploring these two extreme possibilities, the authors find that the conventional prediction (i.e. higher virulence is optimal in co-infection) holds when parasites affect only host mortality. In fact, when more than four parasites are present, the only stable equilibrium is at the highest possible parasite virulence. In contrast, the opposite pattern emerges when parasite growth affects host growth but not host mortality. Host growth rate still becomes very low (almost zero) in the case of multiple infections, but slow parasite growth remains optimal. In both cases, transmission rates are maximized at low growth rates, because they allow the longest period of parasite growth before hosts die and release parasites for transmission.

Though the results presented in this paper are for the two extremes (i.e. only sub-lethal or only lethal effects), many parasites have both lethal and sub-lethal effects. These combinations could be incorporated by the model, simply by choosing different combinations of parameters a and b. Further, in this formulation, parasite growth was determined by host size, but host “growth” could be generalized to be a reflection of host quality. These minor modifications mean that the conceptual model presented here could be used in a variety of contexts of multiple infection.