Insect virus transmission: different routes to persistence

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Highlights

  • Deep sequencing has allowed for the identification of a large number of covert virus infections in insects.

  • The molecular basis of behavioural changes that facilitate horizontal transmission of some baculoviruses have been identified.

  • We have better theoretical understanding of the evolution of covert infection strategies.

  • Molecular mechanisms leading to persistent infections are coming to light.

Transmission is a fundamental process in disease ecology; however, the factors that modulate transmission and the dynamical and evolutionary consequences of these factors in host populations are difficult to study in natural settings. Much of our current knowledge comes from a limited number of virus groups and few ecological studies. Alternatively, progress has been made in the detection of new viruses and in probing the molecular basis of behavioural manipulation of hosts that might influence virus transmission. An expanding theoretical framework provides guidelines on the conditions under which particular transmission strategies might evolve, and their dynamical consequences, but empirical tests are lacking.

Introduction

Transmission to new hosts is a fundamental process in disease ecology as it determines the long-term persistence of a pathogen within its host population. Pathogen transmission can be divided into two broad categories: vertical transmission, the transfer of a pathogen between parent and offspring and horizontal transmission, the passage of virus among individuals who are not parent and offspring (Figure 1). Viruses have a range of strategies to locate and invade new hosts. Pathogen transmission strategies and their impacts on disease dynamics and virulence levels are active areas of empirical and theoretical research.

Research on the roles and impacts of different transmission strategies in insect pathogens is still sparse although a good theoretical framework has been developed to explore the factors which modulate the role pathogens play in insect dynamics. Long-term data collected under realistic conditions are required however to test these models. Progress has also been made in the development and application of tools to probe insect populations for viruses, and in understanding the molecular basis of virus-induced changes in host behaviour that facilitate virus transmission. A particular challenge is understanding the process of vertical transmission and the means by which viruses can form asymptomatic, covert infections, although molecular evidence now provides potential mechanisms for the switch between latency and active virus replication (see also Asgari, this issue). These areas are the focus of this review.

Section snippets

Insect viruses  new viruses and cryptic communities

Insects host a huge diversity of viruses; however, few have been studied in detail. The origins of insect virology lie in the investigation of diseases of species of commercial interest, primarily the silkworm and more recently bees, and in the development of viruses (primarily baculoviruses) as biological control agents for insect pests. Much of what we know about insect virus ecology is based on baculoviruses [1, 2]. However, information on this group of DNA viruses, which is somewhat unusual

Horizontal transmission  moderating factors and tritrophic effects

Horizontal transmission in insect viruses often occurs through the ingestion of contaminated food via the susceptible feeding stages of insects, although examples of cannibalism, sexual transmission and even vectoring occur. Factors that can potentially influence horizontal transmission of nucleopolyhedrovirus (NPV) and its impact on host dynamics have been explored with small-scale experiments and mathematical models, particularly in the gypsy moth-NPV system (e.g. [9, 10]). But field

Pathogen-induced changes in transmission behaviour

One of the fascinating features of many parasites is that they can alter host behaviour after infection, in order to increase the likelihood of their transmission (see also Pinheiro et al., this issue for plant virus modulation of vector behaviour). Such behavioural changes have been shown in insect viruses, primarily baculoviruses. For example, NPV infected larvae in some species have increased activity and climb up the plant to die, which increases dissemination of virus occlusion bodies to

Vertical transmission

It is not clear how many viruses rely solely on vertical transmission for their persistence. At one extreme there are the polydnaviruses, a large group of viruses found in a mutualistic relationship with braconid and ichneumonid wasps [30]. The transmission of these viruses is totally tied to the reproduction of their wasp host as a provirus is incorporated in the wasp genome (known as an endogenized viral element) and only replicates in the wasp. The wasp injects polydnavirus particles

Mixed mode transmission

Many other insect viruses, including baculoviruses, iridoviruses and cypoviruses, can be transmitted both horizontally and vertically, but the prevalence of each route varies. For example, most bee viruses (which are RNA viruses belonging to the Picornavirales) persist as covert infections; however, there is also evidence that infection can be introduced horizontally via contaminated food [33]. Bee viruses are unusual in the insect world in that they can also be vectored: the introduction of

What maintains different transmission strategies?

One of the most interesting questions is why viruses have evolved this array of transmission routes. For example, in a virus that can be transmitted by both horizontal and vertical transmission, under what conditions is each strategy likely to predominate?

Concluding remarks

The understanding of insect virus ecology is progressing, but at a slower rate than advances in other areas. Although improvements in sequencing technology and genomics provide tools that could be used to address many outstanding questions relating to disease transmission, field studies and long-term data are required to elucidate the persistence of different viruses, and communities of viruses over time. Persistence of viruses is still a key question, as is how they interact with competing or

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

I would like to acknowledge the Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grants programme for support and Judy Myers for comments on the manuscript. I am very grateful to Grant Olson for letting me use his excellent western tent caterpillar illustrations in Figure 1.

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