In sickness and in health: RNA-Seq finds viruses associated with mutualist quality in the Amazonian plant-ant Allomerus octoarticulatus

Ant-plant symbioses are classic examples of mutualism in which ant "bodyguards" defend myrmecophytic plants against enemies in exchange for nest sites and often food. We used RNA-Seq to profile the transcriptomes of Allomerus octoarticulatus ant workers, which aggressively defend the Amazonian plant Cordia nodosa against herbivores, but to varying degrees. Field behavioral assays with herbivores in the Peruvian Amazon showed striking variation among colonies in the relative zeal with which A. octoarticulatus workers defend their host plant. Highly effective and ineffective bodyguards differed in their gene expression profiles, which revealed viral infections significantly associated with ant bodyguarding behavior. Transcripts from eight new positive-sense single-stranded RNA viruses were differentially expressed between colonies with high- or low-quality bodyguards. Colonies of high- and low-quality bodyguards were infected by distinct viruses, including viruses clustering phylogenetically with viruses known to cause aggression or reduced locomotion, respectively, in bees. Gene expression, including of immunity-related genes, also differed between broodcare workers and bodyguard ants, suggesting bodyguarding is a distinct worker task. Ant colony health and viral infections may influence ant cooperation with plants in ant-plant mutualisms. Significance statementMany animals have evolved to cooperate with plants in plant-animal mutualisms, including in pollination, seed dispersal, and defensive ant-plant interactions. Although the ecology of these interactions is well studied, little is known about the molecular mechanisms involved in animal cooperation with plants. Studying an Amazonian ant-plant symbiosis, we combined field assays of ant behavior with RNA-Seq to profile the transcriptomes of ants that vary in their quality as defensive plant "bodyguards." Bodyguard ants that effectively defended plants against herbivores expressed different genes than both ineffective bodyguards and broodcare workers. Surprisingly, many genes differentially expressed between high- and low-quality bodyguards were from viruses, and not ants. Thus, we linked viral infections to mutualist quality in this ant-plant symbiosis.