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

Bryan J. Cassone, Andrew P. Michel, Lucy R. Stewart, Raman Bansal, Rouf Mian, Margaret G. Redinbaugh
Genome Biology and Evolution 2014 v.6 no.4 pp. 873-885
Aphis glycines, Bean pod mottle virus, Glycine max, Soybean mosaic virus, bioassays, fecundity, gene expression regulation, insect pests, insect vectors, invasive species, messenger RNA, mortality, parthenogenesis, phenotype, plant viruses, soybeans, tritrophic interactions, virus replication
Pathogens and their vectors have co-evolutionary histories that are intricately intertwined with their ecologies, environments and genetic interactions. The majority of non-persistently transmitted plant viruses are transmitted by aphid species. One important aphid vector in soybean-growing regions of North America is the soybean aphid, Aphis glycines, which transmits at least thirteen plant viruses. In this study we carried out fitness bioassays to examine any impacts on A. glycines survival and fecundity that were conferred by feeding on soybean infected with a virus it transmits (Soybean mosaic potyvirus) and does that it not transmit (Bean pod mottle comovirus). The genetic underpinnings of any observable changes in fitness phenotype were explored using RNA-Seq. Strikingly, feeding on BPMV-infected soybean elicited a large and persistent downregulation of A. glycines transcripts involved in regular cellular activities, and was coupled with significant reductions in aphid fecundity. Although molecular signatures suggested a Small Regulatory RNA pathway defense response is inactivated in aphids feeding on infected plants, BPMV is apparently not replicating in the vector. These results suggest a trade-off between the high energetic cost of parthenogenic reproduction versus the survival benefits of reducing reproduction and other core cellular processes in A. glycines fed on BPMV-infected plants. Ultimately, the inability of A. glycines to adapt to BPMV-infected plants may reflect the short tritrophic evolutionary histories between the insect, plant and virus.