Symbiotic entrenchment through ecological Catch-22

ABSTRACT Symbiotic organisms frequently evolve obligate dependencies on hosts, but the evolutionary changes that entrench such lifestyles are poorly understood. Ant societies are vulnerable to parasitic “myrmecophiles”: impostor species that infiltrate colonies and are often unable to survive outside of them. Here we show that obligate dependence of a myrmecophile on its host arises from irreversibility of the fundamental steps that achieve social acceptance inside the nest. We report a convergent system in which parallel rove beetle lineages (Staphylinidae) evolved from free-living ancestors to parasitize the same host ant. Exploiting this system, we uncover cellular mechanisms by which these beetles mimic host ant cuticular hydrocarbons (CHCs): nestmate recognition pheromones, which function pleiotropically to prevent desiccation. We present evidence of a biological stealth mechanism in a rove beetle in which the CHC biosynthetic machinery becomes transcriptionally silenced on entering the nest. Silencing transforms the beetle into a chemical blank slate onto which ant CHCs are horizontally transferred via interspecies grooming behavior. This strategy leads to identical chemical resemblance and seamless social integration within the colony. CHC pathway silencing is irreversible, however, forcing the beetle into a chronic, physically close dependence on ants to both maintain nestmate status and prevent desiccation. Loss of CHC silencing renders the beetle detectable to ants; conversely, loss of behavioral attraction to ants renders the beetle desiccation prone. Our findings show how symbiotic entrenchment can arise from a Catch-22-like ratchet operating at the organismal level.