Consequences of double virus infections on host plant preference and performance of Aphis gossypii (Hemiptera: Aphididae)

Understanding virus-vector-host interactions in the context of mixed infections is crucial to predict virus spread and develop effective control measures in economically important crops. The virus transmission process plays a central role in plant disease epidemiology and is particularly influenced by vector behavior and life-history traits. However, how mixed virus infections shape vector fitness and host preference remains poorly understood. Here, we determined the effects of double infections with the noncirculative cucumber mosaic virus (CMV, Cucumovirus) and the circulative cucurbit aphid-borne yellows virus (CABYV, Polerovirus) on the fitness and host plant preference of the aphid Aphis gossypii Glover on the host plant, melon (Cucumis melo L.). We revealed that aphids feeding on melon infected only with CMV (single-infected) weighed less and had lower fecundity than those feeding on uninfected plants or CABYV single- or double-infected plants. The mean relative growth rate and, consequently, the intrinsic rate of natural increase were also lower in aphids on CMV single-infected plants, indicating a negative impact of CMV single-infection on aphid fitness. In choice experiments, aphids were initially attracted to CABYV/CMV double-infected plants, but this was followed by a shift in host preference toward mock-inoculated plants over time. These findings suggest that mixed infections can modulate vector behavior in complex and dynamic ways. The pattern of early attraction followed by dispersal appears to promote CMV spread while having limited consequences for CABYV transmission, indicating an asymmetrical benefit between these 2 viruses.