Natural enemies mediate the impact of plant microbiota on insect-borne virus transmission

When only some hosts are protected from disease vectors, disease spread may be inhibited through a net reduction in vector visits or amplified as vectors redirect their attention to unprotected hosts. Two factors that determine which outcome prevails are host microbiota that alter vector host-seeking behavior and natural enemies that redistribute or suppress vector populations. Because both shape the frequency and distribution of vector visits, they are essential for understanding how individual-level protection scales to population-level disease dynamics. Yet, how these processes interact across scales remains poorly understood. Pea aphids are major virus vectors in pea crops and are commonly managed using parasitoid wasps. Recent evidence suggests that epiphytic bacteria in the genus Pseudomonas can also repel or kill pea aphids, yet whether Pseudomonas complements or undermines parasitoid-based vector control remains unknown. We used a mathematical model to show when and why Pseudomonas complements versus undermines biocontrol of aphid-vectored virus outbreaks. The effect of Pseudomonas on virus outbreaks depends most strongly on how successful parasitoids are at tracking aphid densities: When parasitoids effectively track aphids, Pseudomonas inhibits virus outbreaks by reducing aphid densities. With poor parasitoid tracking of aphids, Pseudomonas-induced aphid mortality generates spatial variability in aphid densities that slows parasitoid population growth. The net result is amplified crowding in plants not protected by Pseudomonas, increasing winged aphid production and accelerating viral spread. Counterintuitively, the more effective Pseudomonas is at killing aphids, the more strongly it generates spatial variability and promotes virus spread. The only other factor that can change the direction of Pseudomonas effects on virus outbreaks is whether the virus starts on a Pseudomonas-protected plant, which can cause Pseudomonas to inhibit virus outbreaks when it would otherwise promote them. Our results show how community and spatial context dictate whether microbiota protective to individual hosts will accelerate viral outbreaks.