Studies of the effects of natural selection on disease resistance typically focus on the conditions under which selection will favor increasing, decreasing, or stable levels of resistance.  Here we instead ask, how does natural selection on disease resistance affect host-pathogen population dynamics?  Our immediate interest is in understanding the role of natural selection in forest-insect outbreaks.  Forest-insect outbreaks are often terminated by epidemics of fatal baculovirus pathogens, which can cause extremely high mortality.  In standard models of pathogen-driven outbreaks, some variability in resistance is required to avoid unstable oscillations that lead to extinction of the pathogen.  Sufficiently high levels of variability, however, produce a stable equilibrium, which is equally unrealistic.    Previous work in our lab has shown that variability in disease resistance among gypsy moth larvae is high enough to produce a stable equilibrium in standard models, which is completely at odds with the periodic outbreaks typical of North American gypsy moths.  The standard models, however, assume that disease resistance is entirely determined by environmental factors.  Here we use a combination of field transmission experiments and mathematical models to suggest that natural selection on disease resistance may play a key role in insect outbreaks.

Results/Conclusions

Our initial experiments showed that gypsy moth populations from different years and areas vary widely in their resistance, as measured by risk of infection in transmission experiments.  Further experiments showed that resistance generally falls after population crashes, because of the high disease mortality that occurs during crashes.  Further experiments provided at least modest evidence that resistance is heritable, and observational data suggest that there may be costs of resistance.  We therefore extended the standard models to allow disease epidemics to drive increases in resistance as populations crash, and to allow a cost of resistance to drive reductions in resistance when infection rates are low between outbreaks.  The resulting model shows realistic cycles even for high levels of variability in resistance, suggesting that natural selection on disease resistance may play a key role in gypsy moth outbreaks.  Estimates of heterogeneity in disease resistance in other forest-insect hosts are similarly high, suggesting that resistance evolution may generally be important in insect-pathogen interactions.  More generally, our results provide a clear example of how natural selection can affect complex population dynamics in host-pathogen interactions.  We are currently extending this work to allow for the evolution of pathogen virulence.