Epidemiological and ecological consequences of virus manipulation of host and vector in plant virus transmission

Abstract

Many plant viruses are transmitted by insect vectors. Transmission can be described as persistent or non-persistent depending on rates of acquisition, retention, and inoculation of virus. Much experimental evidence has accumulated indicating vectors can prefer to settle and/or feed on infected versus noninfected host plants. For persistent transmission, vector preference can also be conditional, depending on the vectors own infection status. Since viruses can alter host plant quality as a resource for feeding, infection potentially also affects vector population dynamics. Here we use mathematical modelling to develop a theoretical framework addressing the effects of vector preferences for landing, settling and feeding - as well as potential effects of infection on vector population density - on plant virus epidemics. We explore the consequences of preferences that depend on the host (infected or healthy) and vector (viruliferous or nonviruliferous) phenotypes, and how this is affected by the form of transmission, persistent or non-persistent. We show how different components of vector preference have characteristic effects on both the basic reproduction number and the final incidence of disease. We also show how vector preference can induce bistability, in which the virus is able to persist even when it cannot invade from very low densities. Feedbacks between plant infection status, vector population dynamics and virus transmission potentially lead to very complex dynamics, including sustained oscillations. Our work is supported by an interactive interface https://plantdiseasevectorpreference.herokuapp.com/. Our model reiterates the importance of coupling virus infection to vector behaviour, life history and population dynamics to fully understand plant virus epidemics. AUTHOR SUMMARYPlant virus diseases - which cause devastating epidemics in plant populations worldwide - are most often transmitted by insect vectors. Recent experimental evidence indicates how vectors do not choose between plants at random, but instead can be affected by whether plants are infected (or not). Virus infection can cause plants to "smell" different, because they produce different combinations of volatile chemicals, or "taste" different, due to chemical changes in infected tissues. Vector reproduction rates can also be affected when colonising infected versus uninfected plants. Potential effects on epidemic spread through a population of plants are not yet entirely understood. There are also interactions with the mode of virus transmission. Some viruses can be transmitted after only a brief probe by a vector, whereas others are only picked up after an extended feed on an infected plant. Furthermore there are differences in how long vectors remain able to transmit the virus. This ranges from a matter of minutes, right up to the entire lifetime of the insect, depending on the plant-virus-vector combination under consideration. Here we use mathematical modelling to synthesise all this complexity into a coherent theoretical framework. We illustrate our model via an online interface https://plantdiseasevectorpreference.herokuapp.com/.