Understanding the mechanisms of persistence and dispersal of an insect pathogen and its potential for novel strategic control of African armyworms

African armyworm, the caterpillar of the African armyworm moth, is a major migratory pest in Africa; similar to locusts in its devastation of crops and grasslands, but much more frequent. In countries like Tanzania, where the outbreaks start, armyworms are a problem in 9 years out of 10. In each outbreak, eggs laid by moths hatch into extremely dense swarms of caterpillars that feed voraciously on maize, rice, sorghum and other grain crops. After completing their development, the caterpillars form new swarms of moths that migrate to new areas to start other outbreaks. Some years these outbreaks can continue for months, growing in size and spreading out from Tanzania across Africa, following the annual rains and damaging millions of hectares of crops. The current control for armyworms relies on spraying outbreaks with chemical insecticides. However, the high cost means that up to 70% of food producers suffer damage and often total loss of crops. Especially vulnerable are the poor who rely on household maize plots for food. This project aims to investigate a radically new biological approach to controlling armyworm, through the strategic use of a natural armyworm disease - armyworm nucleopolyhedrovirus (NPV). NPV occurs naturally and, late in the season, and can completely wipe out armyworm outbreaks as it spreads from caterpillar to caterpillar. However, in most years the disease appears too late in the armyworm season to prevent most outbreaks and crop damage. Previous work has shown that NPV is specific to armyworm and so is safe to humans, livestock and wildlife. Field trials have shown that it can be sprayed onto armyworm outbreaks to start disease epidemics, and so could be used as an effective alternative to chemical insecticides. We have shown that the virus can easily be mass produced by harvesting dead larvae from sprayed outbreaks and cheaply formulated into a biological insecticide ready for spraying new infestations. This new project will study the natural biology of NPV in armyworms, focussing on how it spreads and persists in armyworm populations. Using this information, we will determine whether we can prevent the spread of armyworms from the first outbreaks of the year, by manipulating virus populations and so preventing crop damage and the need for expensive chemical control. This will involve a major study on the genetics of the virus, and will require a deeper understanding of how the virus interacts with its host at the cellular, individual and population level. NPV is normally a highly-infectious acute disease, capable of spreading rapidly and killing insects within 3-4 days. A particularly fascinating aspect of NPV is that, when armyworms are scarce during the dry season, the virus can switch into a non-lethal form that can persist inside insects and be transmitted to their offspring via the eggs. Later, when the rains return and dense swarms of caterpillars start to appear, the disease seems able to re-activate itself into the highly-infectious lethal state. We hope that by understanding how disease epidemics occur, and when they might be absent, we can help African scientists to better predict when crops are at risk, and when the scale of armyworm outbreaks are likely to require control. Also, we hope that we can prevent the spread and migration of this serious crop pest across Africa, either by triggering the switch between the lethal and non-lethal forms of the virus, and/or by applying NPV to the earliest outbreaks, so bringing them under control. By studying this natural biological control of this major pest, we hope to reduce or eliminate this threat to the food supply of millions of poor farmers and their families in Africa, save developing countries millions of dollars in control costs, while at the same time reducing the need to apply environmentally-damaging chemicals to some of the most important areas of biodiversity and wildlife conservation in Africa.

Baculoviruses show promise as strategic pest control agents because of their: low environmental impact; propensity for self-replication; and propensity to survive as sub-lethal, vertically-transmitted, persistent infections. This proposal explores some of the assumptions of strategic control by examining the interaction between an important insect crop pest, African armyworm (AAW), and its endemic virus (SpexNPV). Early season AAWs occur in outbreak areas in S. Tanzania. When these larvae develop into adult moths, they fly 100s of km to initiate outbreaks elsewhere in Tanzania. This process continues during the rainy season, spreading throughout Africa. Late-season outbreaks may be naturally controlled by SpexNPV, but this usually occurs too late in the seasonal cycle to limit crop damage. Due to its high pathogenicity to AAWs, SpexNPV is being developed as a microbial insecticide for use in Tanzania. We will study the long-term spatio-temporal dynamics of AAW, using 30 years of data on the incidence of larval outbreaks and adult moth numbers, allowing us to identify environmental factors affecting moth dynamics and the locations of early-season 'source' populations. We will examine spatial and temporal patterns in the virus population, by assessing SpexNPV prevalence in outbreaks throughout Tanzania. We believe a major contributor to the pattern of virus epidemics is the rate at which sub-lethal, persistent SpexNPV infections convert to overt, lethal ones. We will explore potential 'triggers' for this conversion, ask in which tissues the persistent virus resides, how it is vertically transmitted, and whether this can be exploited in strategic control. We will examine the molecular genetics of persistent and overt viral infections to determine the degree of spatial genetic structure within the virus population. We will also explore whether the virus displays any genetic or phenotypic variation within years, indicating within-season selection acting on SpexNPV.