Reduction in fecundity and shifts in cellular processes by a native virus on an invasive insect

Pathogens and their vectors have coevolutionary histories that are intricately intertwined with their ecologies, environments, and genetic interactions. The soybean aphid, Aphis glycines, is native to East Asia but has quickly become one of the most important aphid pests in soybean-growing regions of North America. In this study, we used bioassays to examine the effects of feeding on soybean infected with a virus it vectors (Soybean mosaic virus [SMV]) and a virus it does not vector (Bean pod mottle virus [BPMV]) have on A. glycines survival and fecundity. The genetic underpinnings of the observed changes in fitness phenotype were explored using RNA-Seq. Aphids fed on SMV-infected soybean had transcriptome and fitness profiles that were similar to that of aphids fed on healthy control plants. Strikingly, a significant reduction in fecundity was seen in aphids fed on BPMV-infected soybean, concurrent with a large and persistent downregulation of A. glycines transcripts involved in regular cellular activities. Although molecular signatures suggested a small regulatory RNA pathway defense response was repressed in aphids feeding on infected plants, BPMV did not appear to be replicating in the vector. These results suggest that incompatibilities with BPMV or the effects of BPMV infection on soybean caused A. glycines to allot available energy resources to survival rather than reproduction and other core cellular processes. Ultimately, the detrimental impacts to A. glycines may reflect the short tritrophic evolutionary histories between the insect, plant, and virus.