Resistance: The role of genetic architecture and refuge strategy on the evolution of resistance to Bt-crops in lepidopteran pests

Bt-crops, engineered to express a variety of toxins derived from Bacillus thuringensis, are an efficient method for controlling agricultural insect pests, particularly moth caterpillars. However, as with conventional insecticides, several insect populations around the globe have found ways to evolve mechanisms of resistance to Bt. Therefore, the sustainable use of Bt-crops is dependent on preventing, or at least greatly slowing, the rate at which resistance evolves, and by developing new Bt-crop varieties that target one or more weak points in the pest defences.

Resistance spreads through a population much more slowly when the resistance trait is fully recessive (as opposed to partially recessive or dominant), and when the proportion of susceptible individuals in the population is high (which prevents two copies of the resistance alleles coming together in the same individual). This is why Bt-crops are engineered to deliver a high dose of toxin that is supposed to kill all individuals outright, and they are grown together with non-Bt plants, to sustain a sufficiently large number of susceptible individuals. The problem is that, for various reasons, the assumptions on which this resistance management strategy is based rarely apply to field conditions. This project is about putting these assumptions under the microscope by studying the genetics of Bt resistance in two major moth pests of maize, and incorporating this information into a predictive model to provide a more nuanced basis for designing insect resistance management strategies.

The primary focal species is the African maize stalkborer, the major insect pest of maize and sorghum in sub-Saharan Africa. This project aims to discover the genetic changes that have occurred in the African maize stalkborer population in South Africa to confer dominant resistance to Bt maize, which led to the economic failure and replacement of the original Bt-crop variety. Surveys of genetic diversity will also allow us to assess the risk of Bt-resistance evolving in east African countries, where Bt-maize is close to being released.

The secondary focal species is the Fall armyworm, a major pest of maize and cotton in the Americas, where it has evolved resistance to some Bt toxins. This species colonised west and central Africa in 2016, and has now spread to eastern and southern Africa, where it has elicited emergency large scale pesticide spraying of maize fields. By establishing the degree of tolerance (and its genetic basis) in the South African Fall armyworm population to the Bt-maize currently in use, and plugging this information into our model, we will provide a timely evaluation of how this non-native pest species is likely to cope with the current Bt-resistance management regime in a new ecological setting.

The benefits of this research are that specific knowledge about the genetic identity and diversity of Bt resistance and tolerance mechanisms, when put together with a more realistic model, will aid in making more reliable predictions about the rate of appearance and spread of resistance under alternative refuge design approaches. The results, including comparative analysis of two major pest species, will also contribute to developing new Bt crops that provide longer-term lepidopteran pest control. Finally, the outputs will both provide general scientific insights and be directly relevant to addressing a regional food security problem urgently in need of solutions.

This project aims to integrate new and existing information on the genetic architecture of resistance and tolerance to Bt-crops, within an ecological-genetic modelling framework, to make general predictions about the rate of field-resistance evolution under alternative insect resistance management (IRM) regimes. Such a programme is necessary to improve on existing overly simplistic models, and to resolve the controversy over contrasting IRM strategies (block refuges vs seed mixtures). At the same time, the proposed work is directly relevant to improving maize yields in sub-Saharan Africa, which are severely depressed by lepidopteran pests, together with drought and disease.

The focal species will be the African maize stalkborer (Busseola fusca), the major insect pest of maize and sorghum in sub-Saharan Africa, and the Fall armyworm (Spodoptera frugiperda), an invasive pest of Africa native to the Americas. B. fusca resistance to Cry1Ab toxin in South Africa is of particular interest, as its dominant mode of inheritance does not conform to the widely assumed recessive mode reported in other insects - and was key to its rapid spread, leading to crop failure and replacement of the MON810 variety.

To these ends, we will:
- identify the gene or genes, and ultimately mutation(s), controlling dominant resistance in B. fusca from SA to Cry1Ab toxin);
- identify loci that confer tolerance in naïve populations to sub-lethal doses of single toxin Cry1Ab, and two-toxin Cry1Ab/Cry2Ab2, in B. fusca and S. frugiperda.
- characterise the standing genetic diversity present within Bt-resistance and Bt-tolerance candidate genes in B. fusca populations from SA and Kenya.
- make predictions about resistance evolution under alternative IRM strategies via construction of a demo-genetic model that incorporates empirically informed features of the
genetic architecture, including mode of inheritance (degree of dominance) and genetic diversity, of Bt-resistance and Bt-tolerance.

Maize is the dominant food staple in East and Southern Africa, accounting for 40% of the calories consumed, with per capita maize consumption in the region averaging more than 100 kg/year. Owing to rising demand, driven by rapid population growth, and low yields, sub-Saharan Africa currently imports 2-3 Mt of maize annually. A recent analysis concluded that over the next 20-30 years, in order to achieve 80% cereal self-sufficiency, maize yields, which are currently averaging ~20% of potential, will need to more than double. Achieving this goal will require improved methods of pest and disease control.

Bt-crop technology can be effective against stemborers and armyworms, which cause maize yield losses of 10-80% and threaten regional food security in some cropping seasons. It is crucial however, that the use of Bt-crops be regionally managed to minimize the risk of resistance evolving, as has happened in a few cases. This project will provide recommendations on the optimal deployment of Bt-maize in sub-Saharan Africa, with special reference to controlling its two main insect pests: the African maize stalkborer and the Fall armyworm. This research is particularly timely because Bt-maize is about to be released for the first time in East African countries, and the Fall armyworm invaded Africa in 2016/17. Knowledge exchange will be through publications in high profile publications in the academic and agricultural press, regional conferences on pest management, and two IRM workshops in South Africa and Kenya directed at local stakeholders.