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In addition to individual immunity, social insects have evolved collective defence strategies against pathogens, which consist of behavioural, physiological and organisational adaptations. The importance of social immunity in preventing disease transmission in insect societies is well known. However, we still lack a clear understanding of how collective defence mechanisms are regulated and how they interact with the other regulatory systems of the organism such us the individual immune system. Here we assess how individual immune factors shape the collective immune response to pathogens by inhibiting a key Termite immune effector: gram-negative binding protein (tGNBP-2). tGNBP-2 triggers downstream innate immunity, in addition to cleaving fungal and bacterial pathogens directly in the external environment. We established mini-colonies of Reticulitermes flavipes inside planar arenas where we were able to observe and record hygienic behaviours (i.e. allogrooming and cannibalism) in near-natural nest conditions. Colonies were either treated with the tGNBP-2 inhibitor or a control solution, after which 5 focal workers were introduced into each colony. Focal workers were pre-exposed to either: 1) the fungal pathogen Metharizium anisopliae 2) the t-GNBP-2 inhibitor + M. anisopliae 3) a control solution. Colonies were recorded and the hygienic behaviours performed by nestmates towards focal termites were analysed. We examined the impact of tGNBP-2 inhibition on individual innate immune regulation, in addition to exploring the wider impact of immune suppression on collective social behavioural responses.
Social insects employ a range of behaviours to protect their colonies against disease, but little is known about how such collective behaviours are orchestrated. This is especially true for the social Blattodea (termites). We developed an experimental approach that allowed us to explore how the social response to disease is co-ordinated by multistep host-pathogen interactions. We infected the eastern subterranean termite Reticulitermes flavipes with the entomopathogenic fungus Metarhizium anisopliae, and then, at different stages of infection, reintroduced them to healthy nestmates and recorded behavioural responses. As expected, termites groomed pathogen-exposed individuals significantly more than controls; however, grooming was significantly elevated after fungal germination than before, demonstrating the importance of fungal status to hygienic behaviour. Significantly, we found that cannibalism became prevalent only after exposed termites became visibly ill, highlighting the importance of host condition as a cue for social hygienic behaviour. Our study reveals the presence of a coordinated social response to disease that depends on stage of infection. Specifically, we show how the host may play a key role in triggering its own sacrifice. Sacrificial self-flagging has been observed in other social insects: our results demonstrate that termites have independently evolved to both recognize and destructively respond to sickness.