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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 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.

SUBMITTER: Cunniffe NJ

PROVIDER: S-EPMC8754348 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Blood-feeding arthropods-like mosquitoes, sand flies, and ticks-transmit many diseases that impose serious public health and economic burdens. When a blood-feeding arthropod bites a mammal, it injects saliva containing immunogenic compounds that facilitate feeding. Evidence from Leishmania, Plasmodium and arboviral infections suggests that the immune responses elicited by pre-exposure to arthropod saliva can alter disease progression if the host later becomes infected. Such pre-sensitisation of host immunity has been reported to both exacerbate and limit infection symptoms, depending on the system in question, with potential implications for recovery. To explore if and how immune pre-sensitisation alters the effects of vector control, we develop a general model of vector-borne disease. We show that the abundance of pre-sensitised infected hosts should increase when control efforts moderately increase vector mortality rates. If immune pre-sensitisation leads to more rapid clearance of infection, increasing vector mortality rates may achieve greater than expected disease control. However, when immune pre-sensitisation prolongs the duration of infection, e.g., through mildly symptomatic cases for which treatment is unlikely to be sought, vector control can actually increase the total number of infected hosts. The rising infections may go unnoticed unless active surveillance methods are used to detect such sub-clinical individuals, who could provide long-lasting reservoirs for transmission and suffer long-term health consequences of those sub-clinical infections. Sensitivity analysis suggests that these negative consequences could be mitigated through integrated vector management. While the effect of saliva pre-exposure on acute symptoms is well-studied for leishmaniasis, the immunological and clinical consequences are largely uncharted for other vector-parasite-host combinations. We find a large range of plausible epidemiological outcomes, positive and negative for public health, underscoring the need to quantify how immune pre-sensitisation modulates recovery and transmission rates in vector-borne diseases.

Project description:There is widespread evidence of plant viruses manipulating behavior of their insect vectors as a strategy to maximize infection of plants. Often, plant viruses and their insect vectors have multiple potential host plant species, and these may not overlap entirely. Moreover, insect vectors may not prefer plant species to which plant viruses are well-adapted. In such cases, can plant viruses manipulate their insect vectors to preferentially feed and oviposit on plant species, which are suitable for viral propagation but less suitable for themselves? To address this question, we conducted dual- and no-choice feeding studies (number and duration of probing events) and oviposition studies with non-viruliferous and viruliferous [carrying beet curly top virus (BCTV)] beet leafhoppers [Circulifer tenellus (Baker)] on three plant species: barley (Hordeum vulgare L.), ribwort plantain (Plantago lanceolata L.), and tomato (Solanum lycopersicum L.). Barley is not a host of BCTV, whereas ribwort plantain and tomato are susceptible to BCTV infection and develop a symptomless infection and severe curly top symptoms, respectively. Ribwort plantain plants can be used to maintain beet leafhopper colonies for multiple generations (suitable), whereas tomato plants cannot be used to maintain beet leafhopper colonies (unsuitable). Based on dual- and no-choice experiments, we demonstrated that BCTV appears to manipulate probing preference and behavior by beet leafhoppers, whereas there was no significant difference in oviposition preference. Simulation modeling predicted that BCTV infection rates would to be higher in tomato fields with barley compared with ribwort plantain as a trap crop. Simulation model results supported the hypothesis that manipulation of probing preference and behavior may increase BCTV infection in tomato fields. Results presented were based on the BCTV-beet leafhopper pathosystem, but the approach taken (combination of experimental studies with complementary simulation modeling) is widely applicable and relevant to other insect-vectored plant pathogen systems involving multiple plant species.

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

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