Transcriptomic diagnostics for identifying interactive effects of pesticides, food deficiency, and heat stress on bee health.

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Pollination by bees is essential for the survival of many wild plants and harvesting of many crops. Over recent decades, however, bees have been in decline worldwide. This creates a major risk and potentially a huge cost - the economic value of pollination is estimated to be £430 million per year in the UK alone. Causes for the recent bee declines include habitat loss which reduces access to food, changing temperatures, and exposure to pesticides. Indeed, previously authorised pesticides in fact have unintended impacts on bees, reducing their abilities to forage for food, and ultimately their survival. Three of the most commonly used pesticides were thus suspended in 2013 and banned by the European Commission in 2018.Does this mean that pesticides that remain authorised pesticides are safe for bees? Unfortunately, the manners by which the effects of pesticides are evaluated have been too crude to be certain. To obtain clarity, we will apply a type of molecular medicine approach that has over the past decade dramatically improved treatment and understanding of human diseases. We will apply the new technology to understand the effects of one established neonicotinoid pesticide (acetamiprid), and two new pesticides that have (with some contention) been heralded as "bee-safe" alternatives to the banned neonicotinoids: sulfoxaflor and flupyradifurone. For this purpose, we will perform controlled experiments in which we expose bees to individual pesticides and pesticide combinations - as occurs when neighbouring farms apply different products. Furthermore, we will perform experiments to determine whether the effects of pesticides change when simulating a warmer climate or if food has low nutritional quality - as is common in landscapes dominated by monocultures. Our experiments will be on two common British bee species that are also extensively bred for agricultural pollination: the social large earth bumblebee Bombus terrestris and the solitary red mason bee Osmia bicornis. The "transcriptomic diagnostics" we apply to the bees will provide tens of thousands of measurements per experiment - rather than the handful obtained through traditional approaches. Indeed, we will measure changes in activity levels for each of the 12,000 gene building blocks in brain, flight muscle and a detoxification tissue of bees. This approach is highly sensitive and able to directly detect even subtle changes in the bees' physiologies and metabolisms. Furthermore, because we will measure gene activity in a detoxification tissue as well as brain and muscle, we will be able to determine whether changes in activity level are helping the bees cope with pesticide exposure. Our work will 1) provide urgently needed insight into the effects of these specific pesticides on bees; 2) likely reveal previously unknown effects of authorised pesticides; 3) identify potential differences between these pesticides which are thought to act in similar manners; 4) clarify whether there are "non-additive" interactions between pesticides or with other environmental stressors; 5) whether conclusions about toxicity for one species are representative of another; and 6) unambiguously demonstrate the power and sensitivity of applying the "transcriptomic diagnostics" approach for determining bee health.The biological knowledge we gain through this project will inform regulatory decisions about the currently authorised pesticides. Furthermore, we expect that the approach we develop will fundamentally improve future evaluation of pesticides for research and regulation. Ultimately, both will improve the fates of Britain's bees.