Learning-induced switching costs in a parasitoid can maintain diversity of host aphid phenotypes although biocontrol is destabilized under abiotic stress

Aphid populations frequently include phenotypes that are resistant to parasitism by hymenopterous parasitoid wasps, which is often attributed to the presence of 'protective' facultative endosymbionts residing in aphid tissues, particularly Hamiltonella defensa. In field conditions, under parasitoid pressure, the observed coexistence of aphids with and without protective symbionts cannot be explained by their difference in fitness alone. Using the cereal aphid Rhopalosiphum padi as a model, we propose an alternative mechanism whereby parasitoids are more efficient at finding common phenotypes of aphid and experience a fitness cost when switching to the less common phenotype. We construct a model based on delay differential equations and parameterize and validate the model with values within the ranges obtained from experimental studies. We then use it to explore the possible effects on system dynamics under conditions of environmental stress, using our existing data on the effects of drought stress in crops as an example. We show the 'switching penalty' incurred by parasitoids leads to stable coexistence of aphids with and without H. defensa and provides a potential mechanism for maintaining phenotypic diversity among host organisms. We show that drought-induced reduction in aphid development time has little impact. However, greater reduction in fecundity on droughted plants of symbiont-protected aphids can cause insect population cycles when the system would be stable in the absence of drought stress. The stabilizing effect of the increased efficiency in dealing with more commonly encountered host phenotypes is applicable to a broad range of consumer-resource systems and could explain stable coexistence in competitive environments. The loss of stable coexistence when drought has different effects on the competing aphid phenotypes highlights the importance of scenario testing when considering biocontrol for pest management.