Termite soldiers contribute to social immunity by synthesizing potent oral secretions

Abstract

The importance of soldiers to termite society defence has long been recognized, but the contribution of soldiers to other societal functions, such as colony immunity, is less well understood. We explore this issue by examining the role of soldiers in protecting nestmates against pathogen infection. Even though they are unable to engage in grooming behaviour, we find that the presence of soldiers of the Darwin termite, Mastotermes darwiniensis, significantly improves the survival of nestmates following entomopathogenic infection. We also show that the copious exocrine oral secretions produced by Darwin termite soldiers contain a high concentration of proteins involved in digestion, chemical biosynthesis, and immunity. The oral secretions produced by soldiers are sufficient to protect nestmates against infection, and they have potent inhibitory activity against a broad spectrum of microbes. Our findings support the view that soldiers may play an important role in colony immunity, and broaden our understanding of the possible function of soldiers during the origin of soldier-first societies.

Eating in a losing cause: limited benefit of modified macronutrient consumption following infection in the oriental cockroach Blatta orientalis

“…mRNA libraries were enriched and prepared using a NEXTflexTM Rapid Directional mRNA-seq Kit protocol (Bioo Scientific) before being sequenced on an Illumina NextSeq500/550 platform at the Berlin Center for Genomics in Biodiversity Research (BeGenDiv). Raw data were processed and annotated as described elsewhere (He et al . 2018) (Supplementary file 1).…”

Peptide Hormones in the Insect Midgut

“…The ingested RNA can be absorbed by the gut cells and then transferred to hemolymph (Maori et al, 2019). Compared to other social insects, many of the proteins in oral fluid are related to the regulation of growth, development, and maturation (LeBoeuf et al, 2016;He et al, 2018;Maori et al, 2019).…”

Inhibition of a Secreted Immune Molecule Interferes With Termite Social Immunity

“…For example, externally-secreted molecules derived from the individual immune system, such as toxins, acids and peptides often operate in conjunction with collective behavioral responses to protect groups against infection (Hamilton et al, 2011;Otti et al, 2014), with such molecules likely serving a critical role as a primary barrier to infection (Zasloff, 2002). In ants, termites as well as other social insect groups, behavioral defenses can be supplemented with the secretion and spread of antimicrobial substances onto body surfaces, where they function as a potent external disinfectants (Hamilton et al, 2011;López-Riquelme and Fanjul-Moles, 2013;Otti et al, 2014;He et al, 2018;Pull et al, 2018). Termites in particular can deploy a wide repertoire of social immune responses including alarm behaviors, avoidance, prophylactic, or antimicrobial secretions, burial of dead bodies, necrophagy, mutual grooming, and cannibalism (Rosengaus et al, 1998(Rosengaus et al, , 1999(Rosengaus et al, , 2011Yanagawa and Shimizu, 2007;Chouvenc et al, 2008;Chouvenc and Su, 2010;He et al, 2018;Bulmer et al, 2019).…”

“…In ants, termites as well as other social insect groups, behavioral defenses can be supplemented with the secretion and spread of antimicrobial substances onto body surfaces, where they function as a potent external disinfectants (Hamilton et al, 2011;López-Riquelme and Fanjul-Moles, 2013;Otti et al, 2014;He et al, 2018;Pull et al, 2018). Termites in particular can deploy a wide repertoire of social immune responses including alarm behaviors, avoidance, prophylactic, or antimicrobial secretions, burial of dead bodies, necrophagy, mutual grooming, and cannibalism (Rosengaus et al, 1998(Rosengaus et al, , 1999(Rosengaus et al, , 2011Yanagawa and Shimizu, 2007;Chouvenc et al, 2008;Chouvenc and Su, 2010;He et al, 2018;Bulmer et al, 2019). Antimicrobial secretions in termites are produced by sternal as well as head glands, and can include antimicrobial compounds found in rectal fluids and feces (Rosengaus et al, 2011;Bulmer et al, 2019).…”