Overcoming insecticide resistance using diverse fungal pathogens and variable agricultural landscapes

Successful agriculture requires crop defence against insects. Brazil's agricultural economy suffers annual yield losses of 14.7 billion US$ from insect pests. Indeed, insects consume 10-20% of all global crops whilst growing or in storage. Agriculture relies on widespread chemical insecticide application. Despite extensive research on insecticide application regimes, insecticidal compounds and genetically modified crops, insects continue to evolve resistance against control agents with predictable regularity. The vast scale of Brazilian agriculture and the levels of insecticide use required for pest control have driven resistance evolution in several significant insect pests. Our pump-priming project assesses how 'biopesticide' fungi that naturally kill insects can be used to sustainably control a major new pest of many Brazilian crops, the invasive cotton bollworm, Helicoverpa armigera.

The logic for our project comes from evolutionary science and the particular features of host-pathogen interactions. Insecticide resistance evolution occurs when a single control agent is applied over a broad area, then consistent evolutionary pressures drive previously-rare resistance genes to spread rapidly through the pest population. To prevent this, our project studies how multiple fungal pathogen strains can be used in a spatial matrix across agricultural landscapes, so that selection for resistance varies in different locations, preventing a uniform evolutionary response. On its own, this approach may not be sufficient because of cross resistance: genes making pests resistant to one fungal strain could also confer resistance to others. However, in host-pathogen systems, the optimum genotype to defend against one pathogen is often highly sensitive to the organism's environment. Simultaneous manipulation of an environmental landscape variable (the type of crop grown by farmers) will substantially decrease the consistency of selection: we predict this will prevent resistance evolution.

To develop a pest control system using these principles, our pump priming project integrates research in Brazil and the UK to:

1. Quantify the extent to which genes making cotton bollworm resistant under one combination of fungal pathogen and crop plant make them susceptible in another pathogen-crop combination. We will measure these genetic relationships in a large lab experiment, taking many pest genotypes, allowing each to feed on one of three crops, then exposing them to different fungal strains.

2. Establish that multiple fungal pathogen strains can kill cotton bollworm larvae and have desirable pest control properties: e.g. rapid kill rate, feeding suppression, and negative effects on adult survivors. We will do this by testing larval responses to many fungal isolates in the lab.

3. Show that fungal pest control qualities are maintained under temperature and humidity conditions commonly occurring in Brazilian fields. Lab infection experiments will manipulate environmental variables and assess larval mortality. Then we will spray spores onto crops in the field and test how viability and pest pathogenicity degrade over time.

After this pump priming phase, our future work will assess: spatial scales for deploying crop types and fungal biopesticides to block resistance evolution; details of potential evolutionary responses in pests; and economics of implementation.

The whole project will generate a suite of fungal pathogens and recommendations for their application in managed agricultural landscapes comprising multiple crop species to block resistance evolution. With these outputs and our industry/NGO partners we will commercialise a cost effective, practical and evolution-proof pest control system for Brazil.

Our work has several clear beneficiaries. We summarise them below, along with explanations for how each will benefit.

Farmers and the farming economy

Our ambition to develop a sustainable system of pest management using fungal biopesticides will benefit individual farmers and the broad agricultural economy. Farmers will be able to better control insect pests, and consequently harvest higher yields, while the increased stability achieved by decreasing susceptibility to resistant herbivore outbreaks will minimize losses and insurance claims, and reduce overall volatility in the agricultural sector. If our project is successful, the benefits could extend well beyond São Paulo State and be useful for the types of agricultural systems across Brazil (and indeed elsewhere globally).


Industrial partners

A sustainable pest control technology presents advantages to the industrial partner(s) who develop formulations from our initial isolates. Although the work involved in formulating fungal biopesticides is not trivial, companies will be much more likely to recover their investments and secure good profits if the technology is applied in a way that minimizes the chance of pest resistance evolution, and therefore secures the long-term financial rewards of investing in research and development on biopesticides. Because increasing environmental complexity may help expose costs of resistance to other pest-control measures, our system may also incidentally help rescue some technologies that are no longer effective thanks to previous insecticide resistance; such an outcome would help not only farmers but also producers of other pest control products that have suffered rapid evolution of pest resistance (e.g. some Bt cultivars).


The wider public

Being able to manage insect pests more predictably is likely to improve food security in both developed and developing nations. If implemented on a wide scale in the future, we expect that a more heterogeneous worldwide agricultural landscape in combination with an arsenal of appropriate biopesticides, will stabilise food prices and help minimize local food shortages that are a source of suffering, inequality and conflict. In addition, the public will benefit from reduced ecological costs of current pest control practices. For example, chemical pesticides are known to have adverse consequences for nontarget organisms living on or near agricultural land. The benefits to ecosystems will pay dividends to the public, because of the many services that healthy ecosystems provide, including to agriculture, for example, in the form of plant pollination and predation of pests.