Inhibition of a Secreted Immune Molecule Interferes With Termite Social Immunity

Abstract

Social immune behaviors are described in a great variety of insect societies and their role in preventing emerging infectious diseases has become a major topic in insect research. The social immune system consists of multiple layers, ranging from the synthesis of external immune molecules to the coordination of individual behaviors into sophisticated collective defensive tasks. But our understanding of how complex group-level behavioral defenses are orchestrated has remained limited. We sought to address this gap in knowledge by investigating the relationship between the external activity of an important immune effector molecule in termites, Gram negative binding protein 2 (GNBP-2) and collective grooming and cannibalism. We reasoned that as an external enzyme capable of degrading entomopathogenic fungi, GNBP-2 can facilitate the spread of pathogenic molecules in the colony, and thus serve to trigger collective defenses in a manner analogous to pathogen-associated molecular signatures (PAMPs) of the individual immune system. To test whether GNBP-2 could play a role in regulating social immune behavior, we experimentally inhibited its fungicidal activity using the glycomimetic molecule, D-d-gluconolactone (GDL) and recorded collective behavioral responses to an infected nestmate. Contrary to expectations, GNBP-2 inhibition did not influence the rate or intensity of grooming of either control or fungus-infected nestmates. By contrast, we found that the probability of being harmed through defensive cannibalistic behaviors was significantly reduced by the inhibition of GNBP-2. Our findings indicate that the regulation of collective immune behaviors may depend in part on the external secretion of an enzyme originating from the individual immune system, but that other cues are also necessary.

Superorganism Immunity: A Major Transition in Immune System Evolution

“…are widespread in non-social insect lineages (Bulmer et al, 2012;Otti et al, 2014;Meunier, 2015). Therefore, initially simple, cooperative behaviors such as grooming, combined with means to deploy disinfectants into the external environment, could both protect the group and encourage further cooperation (Esparza-Mora et al, 2020).…”

Microbial Response to Fungal Infection in a Fungus-Growing Termite, Odontotermes formosanus (Shiraki)

“…However, social and innate immunity are not independent of each other (Liu et al, 2015). Studies have confirmed that social immunity depends in part on the regulation of exogenous enzymes associated with the body's immune system (Esparza-Mora et al, 2020).…”

Evidence for reduced immune gene diversity and activity during the evolution of termites

“…Immune gene components, particularly immune effectors, have been implicated in the evolution of social immunity. In termites, termicins, a defensin-like gene family, has been duplicated during the evolution of termites (Bulmer and Crozier, 2004), while gram-negative bacteria-binding proteins (GNBP) have acquired a novel fungicidal function in the common ancestor of eusocial termites and subsocial wood roaches via gene duplication (Bulmer et al, 2012), and may play a role in termite collective defensive behavior (Esparza-Mora et al, 2020). In contrast, it has also been hypothesized that sociality could lead to relaxed selection on the individual immune system, potentially via enhanced behaviourally-mediated protection (e.g.…”