Symbiotic entrenchment through ecological Catch-22.

Abstract

Why symbiotic organisms evolve irreversible dependencies on hosts is an outstanding question. We report a biological stealth device in a beetle that permits infiltration of ant societies. Via transcriptional silencing, the beetle switches off biosynthesis of cuticular hydrocarbons (CHCs)-body surface pheromones that function pleiotropically as a waxy desiccation barrier. Silencing transforms the beetle into a chemical blank slate onto which ant CHCs are transferred via grooming behavior, leading to perfect chemical mimicry and acceptance into the colony. Silencing is irreversible, however, forcing the beetle into a chronic dependence on ants to both maintain mimicry and prevent desiccation. We show that evolutionary reversion of the silencing mechanism would render the beetle detectable to ants; conversely, reversion of the beetle's attraction to ants would render it desiccation prone. Symbiotic entrenchment can thus arise from epistasis between symbiotic traits, locking lineages into a Catch-22 that obstructs reversion to living freely.