Regulation of a symbiotic species network by a Megalomyrmex guest ant parasite: establishment, maintenance, and threat of breakdown

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Abstract The establishment of social interactions between distantly related species is rare and requires effective communication across different sensory and signaling systems. In social insects, interspecies cohesion is particularly striking given the importance of nestmate recognition and colony defense. Megalomyrmex symmetochus guest ants are central to an emerging symbiotic species network model that encompasses ants, bacteria, and fungi. These guest ants are obligate social parasites of the fungus-growing ant Sericomyrmex amabilis , residing within the host nest, exploiting resources, but also protecting against lethal invaders (i.e., predatory ants). However, how the guest ant locates and maintains community balance in collaboration with their host is not well understood. Here, we provide a natural history account of M. symmetochus , combining field observations, behavioral assays, and microbial data to characterize the chemical and ecological features that underlie this symbiosis network. We show that young, mated M. symmetochus queens eavesdrop on host trail pheromones to locate a nest, and once inside, eavesdrop on host alarm signals. In addition to communicative function, we found that M. symmetochus alkaloid venom is also antimicrobial and may influence the microbial community makeup. Finally, we discuss the timing of alate production and dispersal ability of young queens. This work illustrates how guest ant parasites infiltrate and maintain host networks through multi-functional chemical tools. Framing symbioses within interactive communication processes contributes to the understanding of how complex multispecies symbioses emerge and persist in social insect systems over ecological and evolutionary time.