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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 nesting in soil environments are in constant contact with entomopathogens and have evolved disease resistance mechanisms within a colony to prevent the occurrence and spread of infectious diseases. Among these mechanisms: mutual grooming reduces the cuticular load of pathogens, and burial of cadavers and cannibalism can prevent pathogens from replicating within the group. We explored how the rate and type of collective behavioural response is determined by stepwise infection dynamics operating at the level of the individual. Specifically, we infected the eastern subterranean termite Reticulitermes flavipes with different types of infectious particle and infection route of the entomopathogenic fungus Metarhizium anisopliae and recorded behavioural responses of nestmates to individuals at different times during the progression of infections. As expected, termites groomed conidia-exposed individuals significantly more than controls. Interestingly, grooming was significantly elevated after fungal germination than before, suggesting that pathogen growth cues act as strong stimulators of allogrooming. Conidia-exposed termites were cannibalized, but only after they became visibly ill. By contrast, termites did not groom blastospore-injected individuals more than controls at any time-point following infection. Instead, we found that blastospore-injected individuals were continually cannibalized at a low-level following injection with either viable or heat-killed blastospores, with a marked increase in cannibalism after termites injected with viable blastospores became visibly ill and were close to death. Together, these findings point to the importance of host condition as a cue for social hygienic behavior, and that the host itself appears to emit essential sickness cues that act as targets for its own sacrifice. This demonstrates that termites have independently evolved to both identify and destructively respond to sickness.