Exaggeration and cooption of innate immunity for social defense

Significance

Conventionally, immunology has focused on molecular and cellular mechanisms against pathogens and parasites to ensure survival of individuals. Recently, the notion of social immunity has emerged, which highlights the mechanisms in social animals to combat against pathogens, parasites, and other enemies to ensure survival of their society as a whole. Conceptually, social immunity is analogous to but distinct from individual immunity. However, we discovered that, in the social aphid Nipponaphis monzeni, molecular and cellular immune components of soldier individuals are extremely up-regulated and massively excreted via “body eruption” upon gall breakage, and the “hyperclotting” body fluid repairs the damaged gall for colony defense, which uncovers unexpected molecular, cellular, and evolutionary commonalities across individual immunity and social immunity.

Abstract

Social insects often exhibit striking altruistic behaviors, of which the most spectacular ones may be self-destructive defensive behaviors called autothysis, “self-explosion,” or “suicidal bombing.” In the social aphid Nipponaphis monzeni, when enemies damage their plant-made nest called the gall, soldier nymphs erupt to discharge a large amount of body fluid, mix the secretion with their legs, and skillfully plaster it over the plant injury. Dozens of soldiers come out, erupt, mix, and plaster, and the gall breach is promptly sealed with the coagulated body fluid. What molecular and cellular mechanisms underlie the self-sacrificing nest repair with body fluid for the insect society? Here we demonstrate that the body cavity of soldier nymphs is full of highly differentiated large hemocytes that contain huge amounts of lipid droplets and phenoloxidase (PO), whereas their hemolymph accumulates huge amounts of tyrosine and a unique repeat-containing protein (RCP). Upon breakage of the gall, soldiers gather around the breach and massively discharge the body fluid. The large hemocytes rupture and release lipid droplets, which promptly form a lipidic clot, and, concurrently, activated PO converts tyrosine to reactive quinones, which cross-link RCP and other macromolecules to physically reinforce the clot to seal the gall breach. Here, soldiers’ humoral and cellular immune mechanisms for wound sealing are extremely up-regulated and utilized for colony defense, which provides a striking case of direct evolutionary connection between individual immunity and social immunity and highlights the importance of exaggeration and cooption of preexisting traits to create evolutionary novelties.