Why aphid virus retention needs more attention: Modelling aphid behaviour and virus manipulation in non-persistent plant virus transmission

Plant viruses threaten food security and are often transmitted by insect vectors. Non-persistently transmitted (NPT) plant viruses are transmitted almost exclusively by aphids. Because virions attach to the aphid’s stylet (mouthparts) and are acquired and inoculated via brief epidermal probes, the aphid–virus interaction is highly transient, with a very short aphid virus retention time. Many NPT viruses manipulate their host plant’s phenotype to change aphid behaviour to optimise virus transmission. Epidemiological models of this have overlooked a key feature of aphid NPT virus retention: probing or feeding on a plant causes aphids to lose the virus. Furthermore, experimental studies suggest aphids could possibly inoculate multiple healthy plants within one infective period if they do not feed. Consequences of this for virus manipulation of host plant phenotype have not been explored. Our new compartmental epidemiological model includes both behaviour-based aphid dispersal and infectivity loss rates, and the ability of infective aphids to probe multiple plants before virus loss. We use our model to explore how NPT virus-induced host phenotypes affect epidemic outcomes, comparing these results to representative previous models. We find that previous models behave fundamentally differently and underestimate the benefit of an ‘attract-and-deter’ phenotype, where the virus induces increased aphid attraction to infected plants but deters them from prolonged feeding. Our results also highlight the importance of characterising NPT virus retention upon the aphid during probing. Allowing for multiple infective probes increases disease incidence and the effectiveness of virus manipulation, with implications for epidemic prediction and control.Author summary: Plant viruses can cause devastating disease epidemics. Non-persistently transmitted viruses are almost always vectored (transmitted between plants) by aphids. Experiments show virus infection can affect whether aphids are attracted to plants (by altering how infected plants ‘smell’), as well as whether aphids settle for an extended feed after a brief initial probe (by altering how infected plants ‘taste’). Since virus transmission requires an individual aphid to briefly probe an infected plant followed by one or more healthy plant(s), this strongly affects disease transmission. However, most studies exploring virus epidemics do not account for how aphid feeding behaviour affects how long an aphid holds the virus for, or that an aphid could infect multiple healthy plants before losing the virus. We use mathematical modelling to dissect how these aspects of aphid feeding behaviour affect virus transmission, particularly when viruses manipulate the ‘smell’ and ‘taste’ of plants. We show how previous studies, by omitting crucial aspects of aphid feeding behaviour, underestimate how viruses can promote their own transmission. We also highlight that there are very few experimental studies exploring the number of plants an aphid with the virus can consecutively infect, which is a key parameter affecting the severity of epidemics.