Abnormal energy metabolism can alter foraging behavior in termites in different social contexts

Foraging behavior, as an energy-consuming behavior, is very important for collective survival in termites. How energy metabolism related to glucose decomposition and ATP production influences foraging behavior in termites is still unclear. Here, we analyzed the change in energy metabolism in the whole organism and brain after silencing the key metabolic gene isocitrate dehydrogenase (IDH) and then investigated its impact on foraging behavior in the subterranean termite Odontotermes formosanus in different social contexts. The IDH gene exhibited higher expression in the abdomen and head of O. formosanus. The knockdown of IDH resulted in metabolic disorders in the whole organism, including the impairment of the NAD+-IDH reaction and decreased ATP levels and glucose accumulation. The dsIDH-injected workers showed significantly reduced walking activity but increased foraging success. Interestingly, IDH downregulation altered brain energy metabolism, resulting in a decline in ATP levels and an increase in IDH activity. Additionally, the social context obviously affected brain energy metabolism and, thus, altered foraging behavior in O. formosanus. We found that the presence of predator ants increased the negative influence on the foraging behavior of dsIDH-injected workers, including a decrease in foraging success. However, an increase in the number of nestmate soldiers could provide social buffering to relieve the adverse effect of predator ants on worker foraging behavior. Our orthogonal experiments further verified that the role of the IDH gene as an inherent factor was dominant in manipulating termite foraging behavior compared with external social contexts, suggesting that energy metabolism, especially brain energy metabolism, plays a crucial role in regulating termite foraging behavior. Author summary Foraging behavior plays a key role in collective survival in social insects, as found in termites. Worker termites are responsible for foraging duty and exhibit large foraging areas and long foraging distances, so they need to consume much energy during foraging. It is well established that energy can influence insect behaviors. However, how energy metabolism affects foraging behavior in termites remains unknown. Here, we found that the downregulation of the conserved metabolic gene IDH impaired whole-organism and the brain energy metabolism and further altered foraging behavior, resulting in decreased walking activity but increased foraging success in the termite O. formosanus, which is an important insect pest damaging embankments and trees in China. Additionally, the social context affected brain energy metabolism and obviously changed foraging behavior in O. formosanus, causing a decline in foraging success in the absence of nestmate soldiers and the presence of predator ants. However, the increasing number of nestmate soldiers strengthened social buffering to relieve the negative effect of predator ants on worker foraging behavior. Our findings provide new insights into the underlying molecular mechanism involved in modulating the sophisticated foraging strategy of termites in different social contexts from the perspective of energy metabolism.