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 parameterise and validate the
model with values within the ranges obtained from experimental studies. We
then use it to explore 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 amongst 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 stabilising
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.