Phenology under bottom-up control: change in host quality induces diapause in parasitic wasps

When organisms coevolve, any change in one species can affect phenotypes and ecology of the other species. Upper trophic levels have to synchronize their life-cycle to both abiotic conditions and lower trophic level species phenotypic variations and phenology. The role such interactions play in ecosystems is central, but their mechanistic bases remain underexplored. We tested the effect of seasonal variation in host quality on parasitoid diapause induction by using viviparous and oviparous female morphs of the pea aphid Acyrthosiphon pisum . Aphidius ervi parasitoids from two populations of contrasted climatic origin (harsh vs . mild winter areas) were allowed to parasitize each morph in a split-brood design and were next reared under either fall-like or summer-like temperature-photoperiod conditions. We found that oviparous morphs, present before winter, are cues per se for diapause induction; parasitoids entered diapause at higher levels when developing in oviparous hosts (19.4 3.0%) than in viviparous ones (3.6 1.3%), under summer-like conditions (i.e., when oviparous aphids appear in the fields). This pattern was only observed in parasitoids from the harsh winter area, suggesting local adaptations to variation in host quality as an overwintering cue. Analyses of the relative proportion of forty-seven metabolites and lipid reserves in both aphid morphs produced under the same conditions suggest parasitoids response to be mainly influenced by chemical cues derived from the host, with higher proportion of polyols and sugars, and more fat reserves being found in oviparous morphs. Host physiological state thus varies across the seasons and represents one of the multiple environmental indicators of upcoming detrimental conditions, affecting parasitoid overwintering strategies and diapause. Our results underline coevolutionary processes between hosts and parasitoids in their area of origin, likely leading to phenological synchronization with the environment. We point out the importance of such bottom-up effects for ecosystem functioning and for the provision of ecosystem services such as biological control.