Eco-evolutionary theory and insect outbreaks

Abstract

Eco-evolutionary theory argues that population cycles in consumer-resource interactions are partly driven by natural selection, such that changes in densities and changes in trait values 3 are mutually reinforcing. Evidence that this theory explains cycles in nature, however, is almost nonexistent. Experimental tests of model predictions are almost always impossible because of the long time scales over which cycles occur, but for most organisms, even tests of model assump-6 tions are logistically impractical. For insect baculoviruses in contrast, tests of model assumptions are straightforward, and baculoviruses often drive outbreaks of forest-defoliating insects, as in the gypsy moth that we study here. We therefore used field experiments with the gypsy moth 9 baculovirus to test two key assumptions of eco-evolutionary models of host-pathogen population cycles, that reduced host infection risk is heritable and costly. Our experiments confirm the two assumptions, and inserting parameters estimated from our data into the models gives cy-12 cles closely resembling gypsy moth outbreak cycles in North America, whereas standard models predict unrealistic stable equilibria. Our work shows that eco-evolutionary models are useful for explaining outbreaks of forest insect defoliators, while widespread observations of intense 15 selection imposed by natural enemies on defoliators, and frequent laboratory observations of heritable and costly resistance in defoliators, suggest that eco-evolutionary dynamics may play a general role in defoliator outbreaks. 18 only infection risk given exposure (Altizer et al. 2003). Previous work has therefore not provided 45 robust tests of model assumptions.An underlying problem is that overall infection risk is best measured in the field, but for most host-pathogen interactions, field experiments are impractical. Meanwhile, for the few host-48 pathogen interactions for which experiments have measured infection risk in the laboratory or the greenhouse (Auld et al. 2014, 2013; Henter and Via 1995; Herzog et al. 2007; Zbinden et al. 2008), there are no data demonstrating that population cycles occur in nature. For insect bac-51 uloviruses in contrast, field experiments are straightforward (Elderd 2013), and because of the economic importance of the gypsy moth as an outbreaking forest pest, there are extensive data documenting gypsy moth population cycles (Johnson et al. 2005). 54Previous efforts to explain these cycles, however, have met with limited success. Classical insect-pathogen models require variability in host infection risk to prevent pathogen extinction, but realistically high variability causes the models to produce a stable equilibrium instead of 57 cycles (Dwyer et al. 2000). Extending classical models to allow pathogen transmission to be affected by induced plant defenses leads to models that can explain gypsy moth cycles, but the resulting host-pathogen/induced-defense models require particular spatial configurations of tree 60 species (Elderd et al. 2013), and so cannot explai...