The role of a viral symbiont in the thermal mismatch of host-parasitoid interactions.

High temperature events are becoming more severe with climate change, altering species interactions and ecological networks. Symbionts can influence the thermal tolerance of their hosts, yet the mechanisms underlying these effects are poorly understood. We tested the impact of a high temperature event on the molecular interactions among a caterpillar host, Manduca sexta, its parasitoid wasp, Cotesia congregata, and the wasp's symbiotic virus. As in many host-parasitoid systems, high temperatures are lethal to developing parasitoids, but not hosts. Typically, the parasitoid's viral symbiont immunosuppresses M. sexta. Here, we show that elevated temperatures led to an impairment of this immunosuppression, persisting for days after the event ended. Viral gene expression in the host was altered by heat, with distinct expression patterns tied to the virus's genomic architecture. Specifically, viral transcription varied according to the gene's position on viral circular genomic segments: genes located on circles known to integrate into host DNA exhibited increased or unchanged expression following high temperature exposure, while genes on non-integrating circles showed marked reductions in expression. These results demonstrate that high temperatures can disrupt parasitic immunosuppression, which could help explain the lower thermal tolerance of parasitoids relative to hosts. The genomic structure of the viral symbiont may be associated with these effects, but additional research is needed to evaluate this hypothesis. Our findings highlight the importance of complex interactions between environmental temperature, microbial symbionts and host immunity in the ecological responses of host-parasitoid systems to high temperature events.