Enforced specificity of an entrenched symbiosis

The Metazoa encompasses inordinate lineages of symbionts and ecological specialists that obligately depend on particular hosts. The maintenance and fidelity of these lifestyles are often posited to hinge on sensory tuning to host-derived cues, a paradigm supported by studies of neural function in host-specific models. We experimentally reconstituted a socially complex relationship between an obligately symbiotic rove beetle and its single, natural host ant species, permitting us to probe its sensory basis. We show that cuticular hydrocarbons-the ant's nestmate recognition pheromones-elicit host recognition by the beetle and the execution of ant grooming behavior, enabling the beetle to chemically mimic its host and infiltrate the nest as a parasitic impostor. The beetle also follows host trail pheromones, permitting inter-colony dispersal. Yet the beetle also performs these symbiotic behaviors with non-host ants separated by up to ∼95 million years, is able to socially assimilate into their colonies, and shows minimal sensory preference for its natural host over non-host species. Agent-based modeling reveals that the specificity of the beetle emerges not from sensory tuning but from physiological limits on dispersal and negative fitness interactions with alternative hosts, constraining the otherwise promiscuous beetle to its natural host. Recreating the in silico model with living insects empirically demonstrates specificity arising from these enforcing barriers. Our findings show how entrenched symbioses can obviate selection for taxonomically precise host recognition, with specificity emerging from forces external to the symbiont. Chance realization of latent compatibilities with alternative hosts may facilitate host switching, explaining the diversification and deep-time success of such taxa.