Guest-ant social parasites avoid conflict with social hosts using venom signaling

Communication is a fundamental component of symbiosis but when the interests of sender and receiver are not aligned, manipulative rather than informative signaling, may occur between species. Although honest parasite signals are rarely explored, they could be favored if the host-parasite relationship provides an opportunity for a reduction of mutual costs or an acquisition of mutual benefits. Eusocial insect societies exhibit a unique type of symbiotic lifestyle-parasitism of one social unit (i.e., colony) by another. These social parasites gain resources despite risking repeated, and potentially costly, interactions with hosts. Megalomyrmex symmetochus "guest ant" parasites cohabit, long-term, within the nest of a single colony of Sericomyrmex amabilis, a fungus-farming ant. Although M. symmetochus exploit their stingless hosts for resources, they directly rely on their host colony for survival and reproduction, and thus, have been demonstrated to protect their host colony from threats to the shared nest using venom weaponry. We use behavioral observation of staged host-parasite conflict, lethal-dose assays, and direct venom measurements to show that M. symmetochus uses conspicuous and costly displays of venom during interactions with hosts. Megalomyrmex symmetochus is observed to dispense alkaloid venom directly through stinging, but more frequently, indirectly through airborne venom dispersal of volatile pyrrolizidine alkaloids. We further demonstrate that indirect venom use can alter interaction outcomes if hosts switch to non-aggressive behavioral tactics. We interpret this as an honest signal of the threat of envenomation, which reduces the risk of lethal aggression between heterospecific nestmates. We argue that venom signaling in this system, from parasites to their hosts, benefits both species due to the alignment of interest resulting from two different forms of conditional dependence 1) parasite reliance on host colony persistence and 2) the potential role that the parasites play in defending resources of the host colony. This work also demonstrates that communication strategies to manage conflict can arise in antagonistic partnerships and helps us understand how groups with competing interests are able to coexist.