Evolution of molecular and cellular bases of self-sacrificing gall repair in social aphids

The gall-forming aphid Nipponaphis monzeni is known for an extraordinary social behavior called "self-sacrificing gall repair". When a young gall of N. monzeni is damaged by enemies, monomorphic first-instar soldiers massively discharge large amounts of body fluid from their cornicles, which contain large globular cells (LGCs) full of copious amounts of phenoloxidase (PO) and other proteins and lipids, thereby sealing up the gall breach with coagulated body fluid. To gain insight into evolutionary aspects of the spectacular social trait, N. monzeni was comparatively investigated with allied gall-forming aphids Nipponaphis distyliicola, Nipponaphis distychii, Dermaphis autumna and Quadrartus yoshinomiyai. Comparative transcriptomics identified the gall-repairing PO gene expression in the allied species except Q. yoshinomiyai, but the expression levels were very low. Immunohistochemistry identified the PO localization to the fat body of the allied species. These results suggest the possibility that LGCs were evolutionarily derived from fat body cells and a specific PO family gene was massively up-regulated and co-opted for the gall repair. Lipid composition analysis revealed similarity between the gall-repairing coagulating cornicle secretion of N. monzeni and the defensive sticky cornicle secretion of Q. yoshinomiyai, suggesting recruitment of similar lipidic components for distinct social purposes in different ecological contexts.