Context-dependent mutualist warns host before lethal sting

Interspecific communication occurs in species with long-term associations, such as symbioses, to enhance fitness. Here we investigate the role of communication between a fungus-growing ant host, Sericomyrmex amabilis, and their context-dependent “guest-ant” social parasites, Megalomyrmex symmetochus. Guest-ants are long-term obligate associates. Their fitness is reliant on the persistence of their host colony, while host colonies benefit from this association through protection from free-living “raiding-ants”. We hypothesize that a signaling system has evolved to de-escalate conflict between the two symbiotic species (host and guest). In the mercenary-ant system, this may be achieved through a venom-based signal to the host by the parasite. To understand whether venom is a true signal, we performed two studies. First, we assessed the toxicity of parasite venom against host ants using a natural venom and a synthesized alkaloidal proxy (3-hexyl-5-butyl-pyrrolizidine). We then characterized host-parasite behavioral interactions. We find that parasite venom is toxic to the host, but comparative evidence suggests an evolutionary arms-race may be occurring between the host and parasite. Behavioral analyses indicate that parasites more often perform chemical signaling to stinging behavior, and that hosts exhibit submissive behavior in response to both. These results suggest an interspecific chemical communication system has evolved that maintains peace in the nest; which may benefit both the host and parasite species by minimizing fitness costs to each.