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Proc Natl Acad Sci U S A. 2019 Apr 30;116(18):8950-8959. doi: 10.1073/pnas.1900917116. Epub 2019 Apr 15.

Exaggeration and cooption of innate immunity for social defense.

Author information

1
Bioproduction Research Institute, National Institute of Advanced Science and Technology, 305-8566 Tsukuba, Japan; m-kutsukake@aist.go.jp t-fukatsu@aist.go.jp.
2
Bioproduction Research Institute, National Institute of Advanced Science and Technology, 305-8566 Tsukuba, Japan.
3
Computational Bio Big Data Open Innovation Laboratory, National Institute of Advanced Science and Technology, 305-8566 Tsukuba, Japan.
4
Core Research Facilities, National Institute for Basic Biology, 444-8585 Okazaki, Japan.
5
Department of Liberal Arts, The Open University of Japan, 261-8586 Chiba, Japan.
6
Okazaki Institute for Integrative Bioscience, National Institute for Basic Biology, 444-8787 Okazaki, Japan.
7
Life Science Center for Survival Dynamics, Tsukuba Advanced Research Alliance, University of Tsukuba, 305-8577 Tsukuba, Japan.
8
Department of Biological Sciences, Graduate School of Science, University of Tokyo, 113-0033 Tokyo, Japan.
9
Graduate School of Life and Environmental Sciences, University of Tsukuba, 305-8572 Tsukuba, Japan.

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.

KEYWORDS:

hemocyte; phenoloxidase; self-sacrificing gall repair; social aphid; tyrosine

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