Maternal factors from a parasitoid wasp mediate hyperparasitoid attraction to parasitized caterpillars

When parasitizing host caterpillars, parasitoids like Cotesia glomerata not only lay their eggs but also inject symbiotic venom and polydnavirus (CgPDV) that enhance offspring survival by suppressing host immune responses. Parasitism also induces changes in caterpillars that are exploited by hyperparasitoids to locate parasitoid larvae, which serve as hosts for their offspring. However, it remains unclear whether these changes in the caterpillar are driven by the injection of CgPDV, venom or both.

Here, we investigated how CgPDV and venom influence the attractiveness of Pieris brassicae caterpillars to the true hyperparasitoid Baryscapus galactopus . Using a series of choice and non‐choice assays, we quantified hyperparasitoid responses to caterpillars injected with CgPDV and/or venom, compared these with responses to unparasitized caterpillars injected with phosphate‐buffered saline (PBS) and naturally parasitized caterpillars.

We found that B. galactopus preferred caterpillars injected with CgPDV alone or in combination with venom compared with caterpillars injected with PBS. However, the injection of venom alone did not increase the attractiveness of caterpillars to hyperparasitoids. Naturally parasitized caterpillars elicited stronger attraction than any injection treatment, indicating that factors beyond polydnavirus (PDV) and venom contribute to hyperparasitoid attraction. In contrast, neither CgPDV nor venom affected close‐range host‐foraging behaviour of hyperparasitoids, including time until first contact or duration of contact with caterpillars.

These findings demonstrate that parasitoid‐associated PDV contributes to parasitism‐induced changes in caterpillar phenotype that are exploited by a hyperparasitoid, and venom only contributes to this when combined with PDV. Additional parasitism‐related cues are required to fully explain attraction to naturally parasitized hosts. This study provides evidence that an obligate symbiont can mediate multitrophic interactions by indirectly increasing host vulnerability to higher trophic levels.