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

Individual hosts can be protected from disease vectors through their microbiota, but how those benefits scale up to the host population level is rarely obvious. Disease spread may be inhibited through reduced vector visitation or amplified as vectors redirect their attention to unprotected hosts. The outcome--suppression or escalation of disease outbreaks--is likely to be influenced by natural enemies that redistribute or suppress vector populations. The challenge of determining how these processes interact across scales is exemplified by pea aphids, major virus vectors in pea crops that are commonly managed using parasitoid wasps. Recent evidence suggests that epiphytic bacteria in the genus Pseudomonas can repel or kill pea aphids, yet whether Pseudomonas-mediated protection from aphids complements or undermines parasitoid-based vector control remains unknown. We developed a multi-scale mathematical model to investigate why Pseudomonas complements versus undermines biocontrol of aphid-vectored virus outbreaks. Because Pseudomonas-induced mortality leaves aphids patchily distributed, the effect of Pseudomonas on virus outbreaks depends most strongly on how well parasitoids track aphid densities: When parasitoids efficiently locate aphids, Pseudomonas inhibits virus outbreaks by reducing aphid densities. However, when parasitoids are less efficient, they often search unproductively for aphids on Pseudomonas-inhabited plants with few aphids, slowing parasitoid population growth. Reduced parasitism intensifies aphid crowding on Pseudomonas-free plants and boosts the production of winged aphids that accelerate viral spread. Counterintuitively, the more effective Pseudomonas is at killing aphids, the more strongly it generates spatial variability and promotes virus spread. Our results show how community context dictates whether individual microbiota protection slows or accelerates viral outbreaks at the population scale.