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

Abstract

1. 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.2. 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.3. 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. 4. 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. 5. 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. K E Y W O R D S climate change, drought, Hamiltonella defensa, mathematical model, parasitoid, symbiont | 1217 Journal of Animal Ecology PREEDY Et al.

Drought has negative consequences on aphid fitness and plant vigor: Insights from a meta‐analysis

“…Ecological networks often exist in stable equilibria (Landi et al., 2018 ; McQuaid & Britton, 2015 ), with a change in the abundance of one species or functional group leading to perturbations in abundance and diversity across the network (McQuaid & Britton, 2015 ). A drought‐induced reduction in aphid fitness might decrease abundance, mass, or quality of aphids available to support other trophic levels, with potential to destabilize population equilibria; a recent modeling study illustrated that the destabilizing effects of drought on aphid–parasitoid interactions lead to altered insect population cycles (Preedy et al., 2020 ). A key finding of this meta‐analysis was that plant resistance to aphids may influence the extent to which aphids are negatively affected by drought.…”

Towards Predictions of Interaction Dynamics between Cereal Aphids and Their Natural Enemies: A Review

“…Many models represent predation or parasitism dynamics as Type-II or Type-III functional responses [ 57 , 62 ]. Other works recognize the scarcity of available information on certain parameters, such as parasitoid attack rates on aphids, and use their models to explore those parameters’ influences on aphid dynamics by varying their value over realistic ranges [ 63 ].…”

Multiple global change impacts on parasitism and biocontrol services in future agricultural landscapes

“…When other elements of the ecosystem are included, the picture becomes ever more complex. Host feeding on drought-stressed plants may influence symbiont-infected and symbiont-free aphids differently, and speculative modelling work indicates this could disrupt co-existence of symbiont-free and symbiont-infected aphids, with knock-on effects on parasitism (Preedy et al 2020). Impacts of climate change (including temperature and eCO2) on emission of plant volatiles (see above) could interact with known effects of herbivore symbionts on plant volatiles (Frago et al 2017), but experimental evidence of the direction and magnitude of such interactions is currently lacking.…”