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

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.

Flying In-formation: A computational method for the classification of host seeking mosquito flight patterns using path segmentation and unsupervised machine learning

The rational design of effective vector control tools requires detailed knowledge of vector behaviour. Yet, behavioural observations, interpretations, evaluations and definitions by even the most experienced researcher are constrained by subjectivity and perceptual limits. Seeking an objective alternative to ‘expertise’, we developed and tested an unsupervised method for the automatic identification of videotracked mosquito flight behaviour. This method unites path-segmentation and unsupervised machine learning in an innovative workflow and is implemented using a combination of R and python. The workflow (1) records movement trajectories; (2) applies path-segmentation; (3) clusters path segments using unsupervised learning; and (4) interprets results. Analysis of the flight patterns of An. gambiae s.s., responding to human-baited insecticide-treated bednets (ITNs), by the new method identified four distinct behaviour modes: with ‘swooping’ and ‘approaching’ modes predominant at ITNs; increased ‘walking’ behaviours at untreated nets; similar rates of 'reacting' at both nets; and higher overall activity at treated nets. The method’s validity was tested by comparing these findings with those from a similar setting using an expertise-based method. The level of correspondence found between the studies validated the accuracy of the new method. While researcher-defined behaviours are inherently subjective, and prone to corollary shortcomings, the new approach’s mathematical method is objective, automatic, repeatable and a validated alternative for analysing complex vector behaviour. This method provides a novel and adaptable analytical tool and is freely available to vector biologists, ethologists and behavioural ecologists.

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

ABSTRACTMany 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.

Aphid–Plant–Phytovirus Pathosystems: Influencing Factors from Vector Behaviour to Virus Spread

Aphids are responsible for the spread of more than half of the known phytovirus species. Virus transmission within the plant–aphid–phytovirus pathosystem depends on vector mobility which allows the aphid to reach its host plant and on vector efficiency in terms of ability to transmit phytoviruses. However, several other factors can influence the phytoviruses transmission process and have significant epidemiological consequences. In this review, we aimed to analyse the aphid behaviours and influencing factors affecting phytovirus spread. We discussed the impact of vector host-seeking and dispersal behaviours mostly involved in aphid-born phytovirus spread but also the effect of feeding behaviours and life history traits involved in plant–aphid–phytovirus relationships on vector performances. We also noted that these behaviours are influenced by factors inherent to the interactions between pathosystem components (mode of transmission of phytoviruses, vector efficiency, plant resistance, …) and several biological, biochemical, chemical or physical factors related to the environment of these pathosystem components, most of them being manipulated as means to control vector-borne diseases in the crop fields.

Home invasion of triatomines increases the risk of Chagas disease transmission in the Brazilian Amazon

Chagas disease is a parasitic infection with a large reemergent rates in some Amazon regions with usual features of outbreaks of the acute disease mainly by oral transmission. The main vectors of Trypanosoma cruzi are hematophagous insects, the triatomines. Some of them can establish themselves in human dwellings and their annexes but others are mostly wild. In the state of Pará, few records have been made about the occurrence of those wild vectors in fortuitous contact with inhabitants in riverside regions in the Amazon. These vector behaviours have been studied by our group since 2006, trying to explain their role in transmission of the silent disease or asymptomatic infection. The objective of this study is to describe the epidemiological profile of populations exposed to random triatomine home invasion in riverside areas with this registered occurrence. This is a cross-sectional study developed in Abaetetuba city, in the state of Pará, where we conducted a seroepidemiologic survey in inhabitants that registered triatomine home invasion. The results demonstrated that triatomine invasions occur especially in the in-home environment and in the rural zone. The genus Rhodnius was the most found in residences of the municipalities. Direct contact through the vector was reported by 15.55% of the total participants, and an unusual vector behaviour were observed during the day. Despite this small casuistic, 0.47% of the enrolled inhabitants had positive serology IgG anti- T. cruzi antibodies. We confirm one occurrence of asymptomatic infection in a child and, also, favourable links to the Chagas disease transmission chain. Faced with the scarcity of information on triatomine aggression in the Amazon, the authors recommended an entomological study of greater scope in those areas. The record of unusual vector behaviour and the serological surveillance of human populations under this risk may constitute a new tool for the early detection of silent infections and reinforce the knowledges about the behaviour of invading insects. At the same time, health education can assist in strategies for the prevention of Chagas' disease.

Getting ready for integrated vector management for improved disease prevention in Zimbabwe: a focus on key policy issues to consider

Background This paper outlines Zimbabwe’s potential readiness in harnessing integrated vector management (IVM) strategy for enhanced control of vector-borne diseases. The objective is to provide guidance for the country in the implementation of the national IVM strategy in order to make improvements required in thematic areas of need. The paper also assesses the existing opportunities and gaps to promote and adopt the approach as a national policy. Main text Despite recent gains in combating vector-borne diseases, especially malaria, management of vector control programmes still remains insecticide-based and vertical in nature. Therefore, concerns have been raised on whether the current long-standing conventional vector control strategy still remains with sufficient action to continue to break the transmission cycle to the levels of elimination. This is so, given the continuous dwindling resources for vector control, changes in vector behaviour, the emergence of resistance to medicines and insecticides, climate change, environmental degradation, as well as diversity in ecology, breeding habitats, and community habits. Cognizant of all that, elements of a surveillance-driven IVM approach are rapidly needed to move vector control interventions a step further. These include advocacy, policy formulation, capacity building, public and private partnerships, community engagement, and increasingly basing decisions on local evidence. Understanding the existing opportunities and gaps, and the recognition that some elements of IVM are already imbedded in the current health programmes is important to encourage stakeholders to promptly support its implementation. Leveraging on the existing opportunities, combined with sufficient advocacy, IVM could easily be accepted by the Zimbabwe government as part of a wider integrated disease management strategy. The strategy could represent an excellent breakthrough to establish much needed intra and inter-sectoral dialogue, and coordination for improved vector-borne disease prevention. Conclusions After synthesis of the opportunities and challenges clearly presented, it was concluded that it is imperative for Zimbabwe to adopt and implement IVM strategy that is informed by work already done, while addressing the bottlenecks. The significance of refocusing for improved disease prevention that has the potential to accomplish elimination of not only malaria but all vector borne diseases much earlier than anticipated under the existing vector control system is underscored.

Impact of climate change on the occurrence and distribution of bluetongue in Europe

Climate changes may have significant impact on animal health, including changes in the distribution and seasonality of vector-borne diseases. Arboviruses, such as bluetongue virus (BTV), are particularly susceptible to climate change because of their small size and their ability to adapt to variations in the temperature of the environment. Climate also has long-term indirect effects on the transmission of BT via its effects on the distribution and availability of suitable habitats. Changes in BT incidence in Europe have been matched by spatio-temporal changes in regional climates, including the specific climatic drivers of BTV infection. The climate changes are responsible for the occurrence and distribution of BT through their impact on the viral vectors. Changes in climate, i.e. temperature, precipitation, humidity, wind, etc., can influence various aspects of the Culicoides vectors’ life cycle, including survival, population numbers, vector-pathogen interactions, pathogen replication, vector behaviour and, of course, its distribution. Different species of Culicoides have different environmental tolerances, and the optimal temperature and humidity levels for populations of Afro-Asiatic species, such as C. imicola, are different from those for Palearctic species, such as the C. obsoletus and C. pulicaris groups. However, the biotic processes of changing vector roles and distribution have been as important as the climatic process in driving the invasion of Europe by multiple BTV strains. The enhanced transmission of BTV by indigenous European vectors has been instrumental in the spread and persistence of infection in cooler and wetter areas of different regions of Europe after the invasion. The vectorial capacity of Culicoides is dynamic and climate-mediated, making it difficult to state unequivocally that particular species cannot or will not be involved in transmission – even of strains that enter Europe unexpectedly from geographically remote regions. .

Transmission dynamics: critical questions and challenges

This article overviews the dynamics of disease transmission in one-host–one-parasite systems. Transmission is the result of interacting host and pathogen processes, encapsulated with the environment in a ‘transmission triangle’. Multiple transmission modes and their epidemiological consequences are often not understood because the direct measurement of transmission is difficult. However, its different components can be analysed using nonlinear transmission functions, contact matrices and networks. A particular challenge is to develop such functions for spatially extended systems. This is illustrated for vector transmission where a ‘perception kernel’ approach is developed that incorporates vector behaviour in response to host spacing. A major challenge is understanding the relative merits of the large number of approaches to quantifying transmission. The evolution of transmission mode itself has been a rather neglected topic, but is important in the context of understanding disease emergence and genetic variation in pathogens. Disease impacts many biological processes such as community stability, the evolution of sex and speciation, yet the importance of different transmission modes in these processes is not understood. Broader approaches and ideas to disease transmission are important in the public health realm for combating newly emerging infections. This article is part of the themed issue ‘Opening the black box: re-examining the ecology and evolution of parasite transmission’.