Exaggeration and cooption of innate immunity for social defense

Social insects often exhibit striking altruistic behaviors, of which the most spectacular ones may be self-destructivedefensive 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 nymphserupt 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 gallbreach is promptly sealed with the coagulated body fluid. What molecular and cellular mechanisms underlie the self-sacrificing nest repair with body fluidfor the insect society? Here we demonstrate that the body cavityof soldier nymphsis full of highly differentiated large hemocytesthat contain huge amounts of lipid dropletsand phenoloxidase (PO), whereas their hemolymphaccumulates 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 hemocytesrupture 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 gallbreach. 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.