What makes a society dead: accumulation of uric acid increases infectious disease risk in termites

Abstract

In social insect colonies, the high reproductive output of kings and queens is supported by non-reproductive castes, a division of labour that allows for the rapid recovery of individuals, often including those of the reproductive castes. However, these seemingly permanent colonies eventually face collapse. Studying the mechanisms of colony death is crucial for understanding the maintenance of insect social systems. Here, we show that the accumulation of uric acid (a major product of nitrogen metabolism) in workers increases their infectious disease risk in the Japanese subterranean termite Reticulitermes speratus. In this species, king replacement has been associated with colony demise, and we found that king replacement increases the uric acid contents in worker bodies in the field. Uric acid, which has antioxidant activity, was shown to reduce in vivo levels of reactive oxygen species (ROS), a key player in innate immunity. Workers with decreased ROS levels were more susceptible than those with normal ROS levels to an opportunistic pathogen that causes disease to immunocompromised termites. Our results indicate that regulating the individual oxidant/antioxidant balance through the interactions among colony members plays a pivotal role in the immunity of social insects.