The dilution effect among competing, evolving hosts: Doomed by resource competition but rescued by rapid evolution

Background/Question/Methods

Disease outbreaks can simultaneously regulate host population dynamics, shift the balance between competing species, and drive rapid evolutionary change.  We disentangle these eco-evolutionary dynamics while dissecting a current paradigm in disease ecology: the dilution effect.  The dilution effect, broadly defined, predicts a pattern – disease risk decreases when host species diversity increases, through the addition of ‘diluter’ species.  However, these diluter species often compete with focal hosts for resources.  Competition with focal hosts can doom the dilution effect in two ways.  First, if focal hosts compete too strongly, then competitor/diluters (hereafter: friendly competitors) are too sparse to sufficiently interfere with disease spread.  This is especially true when focal hosts drive massive epidemics.  Second, if focal hosts compete too weakly, friendly competitors drive them extinct.  Fortunately, focal host genotypes vary in their competitive ability and magnitude of disease spread, and both of these phenotypes can evolve rapidly.  On the one hand, competition could select for more competitive focal host genotypes, perhaps further dooming the dilution effect.  On the other hand, epidemics could select for more resistant genotypes, perhaps even rescuing the dilution effect by lowering the magnitude of disease spread.  We addressed these uncertainties with experimental algal-zooplankton-fungus mesocosm communities.  

Results/Conclusions

Our mesocosm experiment revealed that the dilution effect was rescued in genetically diverse focal host populations.  Life history traits essential for competition and disease spread were quantified for all 11 focal host genotypes.  The mesocosm experiment manipulated two levels of focal host genetic diversity: high (all 11 genotypes) and low (a subset of 3 genotypes with limited life history trait variation).  Presence of friendly competitors significantly reduced infection prevalence for both genetic diversity manipulations.  However, in host populations with low genetic diversity, this disease reduction came at a strong cost.  Separately, both competition and disease strongly reduced these focal host population densities, presumably because they were unable to respond adequately to competitor-mediated and disease-mediated selection.  Moreover, although the combination of (friendly) competitors and disease did reduce disease prevalence, focal host populations suffered a severe reduction in density.  In some replicates, friendly competition even drove focal hosts extinct.  Alternatively, host populations with high genetic diversity maintained relatively dense populations despite competitor and/or disease-mediated selection.  Thus, although the dilution effect was doomed by resource competition in host populations with constrained genetic diversity, it was rescued by rapid evolution in genetically diverse focal host populations.