Illumination of behavior leading to host exploitation by a context-dependent mutualist

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Parasitic lifestyles are more common than all other lifestyles combined and host-parasite interactions shape food webs, influence behavior, and alter population size and structure. Because insects are widespread, hyper-diverse, and abundant, and most are parasitic, they are ideal subjects for species interaction studies. The proposed study leverages a unique parasite system—easily studied in the field and manipulated in the lab—to address key questions about species interactions. The research objective is to identify behaviors that lead to obligate symbioses (different species living together), while taking into consideration a network of interacting entities (ants, fungus, and bacteria). This comprehensive study is original in its scope, spanning temporal and biological scales, but is also creative in the use of integrative methods (population genetics, morphology, chemical ecology, behavior) to better understand symbiotic relationships. The charismatic Megalomyrmex guest ant/fungus-farming ant host/parasite system has the potential to reshape the way symbioses are perceived while providing a new model that will serve the needs of students and researchers now and in the future. Additionally, these efforts will include students in research and create a bilingual online badge-based educational summer program, led by diverse role models, and centered on conservation of symbioses, enhancing accessibility to STEM education.This study will enable much-needed crosstalk among the fields of parasitology and sociobiology. Megalomyrmex symmetochus is an obligate ‘guest ant’ parasite of a fungus-farming ant, Sericomyrmex amabilis. The costs of hosting guest ants can quickly shift to a net benefit when a more lethal parasite threatens hosts, because the guest ants offer protection through their alkaloidal venom weaponry. Integrative approaches in animal behavior, following a parasitological exploitation framework, will clarify how these context-dependent mutualists influence symbiotic networks. Aims are organized by the stages leading to exploitation, from the initiation of an obligate symbiotic interaction (host-finding/dispersal) (Aim I) to colony integration and species network maintenance (Aims II and III). Aim I compares dispersal ability and population dynamics of hosts and their parasites, capitalizing on flight morphology and population genomics methods. Host-finding strategies will be identified for the first time in a social parasite (one social organism parasitizing another) using a reductionist approach. Not only will ant and fungus garden volatiles be characterized but compounds that attract the host and parasite ants will be discovered. Aims II and III center on parasite venom function. Toxicity and behavioral assays will test if parasitized and non-parasitized ant colonies differ physiologically and behaviorally when exposed to parasite-derived venom alkaloids. 16S metagenomics, culture-based assays, and manipulation experiments will distinguish bacterial symbionts and determine which are susceptible to antimicrobial alkaloidal venom. This work fills a significant gap by identifying how social parasites solve the challenges all parasites face to achieve successful exploitation.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.