Destructive disinfection of infected brood prevents systemic disease spread in ant colonies.

Mark Jf Brown,Thomas Schmitt,Anna V Grasse,Christopher D Pull,Florian Wiesenhofer,Simon Tragust,Sylvia Cremer,Line V Ugelvig

doi:10.7554/elife.32073

Abstract

In social groups, infections have the potential to spread rapidly and cause disease outbreaks. Here, we show that in a social insect, the ant Lasius neglectus, the negative consequences of fungal infections (Metarhizium brunneum) can be mitigated by employing an efficient multicomponent behaviour, termed destructive disinfection, which prevents further spread of the disease through the colony. Ants specifically target infected pupae during the pathogen's non-contagious incubation period, utilising chemical 'sickness cues' emitted by pupae. They then remove the pupal cocoon, perforate its cuticle and administer antimicrobial poison, which enters the body and prevents pathogen replication from the inside out. Like the immune system of a metazoan body that specifically targets and eliminates infected cells, ants destroy infected brood to stop the pathogen completing its lifecycle, thus protecting the rest of the colony. Hence, in an analogous fashion, the same principles of disease defence apply at different levels of biological organisation.

Highlights

Pathogen replication and transmission from infectious to susceptible hosts is key to the success of contagious diseases (Schmid-Hempel, 2011)
We show that the superorganismal societies of ants have evolved an efficient mechanism to target and eliminate infections that have established in colony members, before they become contagious. This is achieved through the detection of chemical cues emitted by infected pupae during the non-transmissible incubation period of the pathogen (Figure 2)
The ants engage in destructive disinfection, a multicomponent behaviour that utilises the ants’ antimicrobial poison, in conjunction with cocoon removal and biting, to prevent pathogen replication within the body of the pupae (Figure 1, Figure 3)

Summary

Introduction

Pathogen replication and transmission from infectious to susceptible hosts is key to the success of contagious diseases (Schmid-Hempel, 2011). Healthy animals usually respond by interacting with sick conspecifics less or avoiding them completely (Poirotte et al, 2017; Kiesecker et al, 1999; Behringer et al, 2006; Anderson and Behringer, 2013). They may prophylactically increase the expression of their immune defences in preparation for a potential immune challenge (Hernandez Lopez et al, 2017), and a similar phenomenon is observed in animals and plants in response to chemicals released by wounded conspecifics (Heil and Silva Bueno, 2007; Peuß et al, 2015).

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Conclusion