Sex makes them sleepy: host reproductive status induces diapause in a parasitoid population experiencing harsh winters

Abstract

When organisms coevolve, any change in one species can induce phenotypic changes in traits and ecology of the other species. The role such interactions play in ecosystems is central, but their mechanistic bases remain underexplored. Upper trophic level species have to synchronize their life-cycle to both abiotic conditions and to lower trophic level species phenology and phenotypic variations. We tested the effect of host seasonal strategy on parasitoid diapause induction by using a holocyclic clone of the pea aphid Acyrthosiphon pisum producing asexual and sexual morphs that are viviparous females (i.e. laying embryos) and oviparous females (laying eggs), respectively, the latter being only present at the end of the growing season. Aphidius ervi parasitoids from populations of contrasted climatic origin (harsh vs. mild winter areas) were allowed to parasitize each morph in a split-brood design and developing parasitoids were next reared under either fall-like or summer-like temperature-photoperiod conditions. We next examined aspects of the host physiological state by comparing the relative proportion of forty-seven metabolites and lipid reserves in both morphs produced under the same conditions. We found that oviparous morphs 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 since low diapause levels were observed in the other population, suggesting local adaptations to overwintering cues. Metabolomics analyses show parasitoids response to be mainly influenced by the hosts physiology, with higher proportion of polyols and sugars, and more fat reserves being found in oviparous morphs. Host quality thus varies across the seasons and represents one of the multiple environmental parameters affecting parasitoid diapause. Our results underline strong coevolutionary processes between hosts and parasitoids in their area of origin, likely leading to phenological synchronization, and we point out the importance of such bottom-up effects for trait expression, and for the provision of ecosystem services such as biological control in the context of climate change.