Pathogenic modification of plants enhances long‐distance dispersal of nonpersistently transmitted viruses to new hosts

Aphids spread the majority of plant viruses through nonpersistent transmission (NPT), whereby virus particles attach transiently to these insects’ probing mouthparts. Virus acquisition from infected plants and inoculation to healthy host plants is favored when aphids briefly probe plant epidermal cells. It is well established that NPT virus infection can alter plant–vector interactions, and, moreover, such pathogen modifications are found in a range of plant and animal systems. In particular, viruses can make plants more attractive to aphids but inhibit aphid settling on infected plants. It is hypothesized that this viral “reprogramming” of plants promotes virus acquisition and encourages dispersal of virus‐bearing aphids to fresh hosts. In contrast, it is hypothesized that virus‐induced biochemical changes encouraging prolonged feeding on infected hosts inhibit NPT. To understand how these virus‐induced modifications affect epidemics, we developed a modeling framework accounting for important but often neglected factors, including feeding behaviors (probing or prolonged feeding) and distinct spatial scales of transmission (as conditioned by wingless or winged aphids). Analysis of our models confirmed that when viruses inhibit aphid settling on infected plants this initially promotes virus transmission. However, initially enhanced transmission is self‐limiting because it decreases vector density. Another important finding is that virus‐induced changes encouraging settling will stimulate birth of winged aphids, which promotes epidemics of NPT viruses over greater distances. Thus our results illustrate how plant virus modifications influence epidemics by altering vector distribution, density, and even vector form. Our insights are important for understanding how pathogens in general propagate through natural plant communities and crops. Aphids vector the majority of arthropod‐transmitted plant viruses and about 30% of known plant viruses (Gray and Banerjee 1999, Brault et al. 2010). Some aphid‐transmitted viruses circulate within vectors and a few can infect insect cells (persistent transmission, PT; for a glossary of specialist terms used in this paper, see Box 1). However, most aphid‐transmitted viruses do not circulate internally and cannot infect the insect. Instead, virus particles attach loosely to the insect's piercing mouthparts (stylets), a form of vectoring called nonpersistent transmission (Gray and Banerjee 1999, Brault et al. 2010; NPT: Box 1). The aphid–NPT virus interaction is ephemeral, and virus particles are rapidly flushed out of the