Abstract
Social insects colonies protect themselves against pathogens by collectively performing disease defences that result in social immunity. As a first barrier to disease, sanitary care between nestmates reduces individual-level exposure and infection. However, if a pathogen overcomes these defences, social insects should have evolved mechanisms to prevent individual infections causing systemic disease spread in the colony. In this study, we investigated how ants prevent disease outbreaks following the successful infection of their brood with a fungal pathogen. We found that the ants can detect lethal infections early in the non-infectious incubation period of the pathogen’s lifecycle, using chemical ‘sickness cues’ expressed by the infected pupae. Following detection, the pupae are unpacked from their cocoons by the ants and bitten to make perforations in the cuticle, through which the ants spray their antimicrobial poison. Since the cocoon and cuticle act as barriers against the poison, this multicomponent behaviour permits the ants to use their poison for internal disinfection of the pupal body, where it can act directly against the proliferating pathogen. We termed this mechanism destructive disinfection as it killed the pupae and prevented pathogen replication. Ultimately, the ants stopped the pathogen from completing its lifecycle and transmitting to new hosts. Thus, destructive disinfection acts as a second line of defence against disease in ant colonies and is analogous to the elimination of infected cells by adaptive immune systems. Our results therefore suggest that pathogen-induced selection can result in similar solutions to common problems across the different levels of biological organisation.