Vector population growth and condition‐dependent movement drive the spread of plant pathogens

Abstract

Plant viruses, often spread by arthropod vectors, impact natural and agricultural ecosystems worldwide. Intuitively, the movement behavior and life history of vectors influence pathogen spread, but the relative contribution of each factor has not been examined. Recent research has highlighted the influence of host infection status on vector behavior and life history. Here, we developed a model to explore how vector traits influence the spread of vector-borne plant viruses. We allowed vector life history (growth rate, carrying capacity) and movement behavior (departure and settlement rates) parameters to be conditional on whether the plant host is infected or healthy and whether the vector is viruliferous (carrying the virus) or not. We ran simulations under a wide range of parameter combinations and quantified the fraction of hosts infected over time. We also ran case studies of the model for Barley yellow dwarf virus, a persistently transmitted virus, and for Potato virus Y, a non-persistently transmitted virus. We quantified the relative importance of each parameter on pathogen spread using Latin hypercube sampling with the statistical partial rank correlation coefficient technique. We found two general types of mechanisms in our model that increased the rate of pathogen spread. First, increasing factors such as vector intrinsic growth rate, carrying capacity, and departure rate from hosts (independent of whether these factors were condition-dependent) led to more vectors moving between hosts, which increased pathogen spread. Second, changing condition-dependent factors such as a vector's preference for settling on a host with a different infection status than itself, and vector tendency to leave a host of the same infection status, led to increased contact between hosts and vectors with different infection statuses, which also increased pathogen spread. Overall, our findings suggest that vector population growth rates had the greatest influence on rates of virus spread, but rates of vector dispersal from infected hosts and from hosts of the same infection status were also very important. Our model highlights the importance of simultaneously considering vector life history and behavior to better understand pathogen spread. Although developed for plant viruses, our model could readily be utilized with other vector-borne pathogen systems.

Species interactions affect the spread of vector‐borne plant pathogens independent of transmission mode

“…Empirical studies also show that predator-vector interactions that affect vector movement and feeding behavior can override consumptive effects on vector abundance (Long and Finke 2015). Although most vector-borne pathogen models track vector abundance, vector movement is often implicit or represented by simple diffusion (McCallum et al 2001; but see Shaw et al 2017Shaw et al , 2019. Our results show that explicit inclusion of movement in models may fundamentally alter predictions.…”

“…) and vector‐borne pathogens (Shaw et al. , ; Roberts and Heesterbeek ), which all show strong effects of transmission efficiency on pathogens. For example, co‐infection of hosts with many pathogens can increase rates of pathogen spread because pathogen–pathogen competition selects for increased transmission efficiency (Alizon et al.…”

The Aphid-Transmitted Turnip yellows virus Differentially Affects Volatiles Emission and Subsequent Vector Behavior in Two Brassicaceae Plants

“…During this stage, aphids exhibit antennal waving on the plant surface, evidently facilitating the detection of odors in the boundary layer close to the plant surface. In this work, the observed contrasted aphid behavior may impact rates of virus spread with implication in virus-disease management [54,55]. In an epidemiological scheme, wild plants or weeds can play a role of virus reservoir and can impact virus propagation.…”

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

“…, Shaw et al. ). However, it is not yet certain that VMPPs are genuine manipulative adaptations (sometimes referred to anthropomorphically as viral strategies) or incidental by‐products of infection (Mauck et al.…”

“…, Sisterson , Shaw et al. ), the central property of NPT, that acquisition occurs when aphids sample epidermal cells of host plants, is omitted because of a focus either on generic or persistently transmitted plant viruses.…”