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 vector's 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.

Highlights

  • Plant diseases have impacts on crops, affecting yield, and on natural plant ecosystems and landscapes, affecting population and community structure [1,2,3]

  • ; εÀ oÀ for persistent transmission (PT) viruses and where for PT we allow the “plus” preference parameters to differ from the “minus” ones, whereas for non-persistent transmission (NPT) related pairs of parameters must be identical

  • HÀ ðS; IÞ 1⁄4 að1 þ dðG À À 1ÞÞ; hþðS; IÞ 1⁄4 að1 þ dðG þ À 1ÞÞ: when β = 1 and δ = 0, i.e. when vector preference does not interact with vector population dynamics, the functions controlling population dynamics become simpler, with gðS; I; X; ZÞ 1⁄4 sðX þ ZÞ

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Summary

Introduction

Plant diseases have impacts on crops, affecting yield, and on natural plant ecosystems and landscapes, affecting population and community structure [1,2,3]. Transmission plays a critical part in disease epidemiology and depends to a large extent on vector life history and behaviour concerning movement, landing, settling, feeding, and reproduction on plants. These aspects are directly linked to the mode of transmission, whether non-persistent, semi-persistent, or persistent [6]. In non-persistent transmission the virus is restricted to the insect’s stylet, in semi-persistent transmission the virus enters the insect’s foregut, and in persistent transmission the virus passes through the gut to the haemolymph and to the salivary glands These modes of transmission can be characterised in large part by the rates of vector acquisition and inoculation and the retention time within the vector [7]. Attempts to determine what drives a plant virus epidemic should aim to characterise the plantvirus interaction, and the plant-vector and virus-vector interactions

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