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Leaf-cutting ants depend on mutualisticfungi to survive. An infection that massively affects the workers compromising the proper maintenance of the fungus, or that can attack the fungus garden, can be fatal to the colony. Thus, leaf-cutting ants have evolved a complex defense system composed of both innate individual immunity and collective immunity to protect the colony against potential threats. To characterize the collective and individual immunity of Atta cephalotes workers to Metarizhium anisopliae we assessed the hygienic behavior and the expression of antimicrobial peptides of A. cephalotes workers triggered by Metarizhium anisopliae spores. As a control challenge, workers were treated with water. Regardless of whether the challenge was with water or spore suspension, A. cephalotes workers displayed an immediate response characterized by an increase in time spent both self-grooming and collective grooming along with a reduction in time spent fungus-grooming. The individual immunity triggered the expression of abaecin as early as 24 hours post-infection, exclusively in workers challenged with M. anisopliae. In contrast, the level of expression of defensin remained constant. These results suggest that upon being challenged with a suspension of M. anisopliae spores, A. cephalotes workers deploy both collective and individual immunity to produce a response against the invader. However, when the spores of M. anisopliae are applied as liquid suspension collective immunity deploys a generic strategy, while individual immunity shows a specific response against this entomopathogen.

Leaf-cutting ants of the genera Atta and Acromyrmex are at constant risk of epizootics due to their dense living conditions and frequent social interactions between genetically related individuals. To help mitigate the risk of epizootics, these ants display individual and collective immune responses, including associations with symbiotic bacteria that can enhance their resistance to pathogenic infections. For example, Acromyrmex spp. harbor actinobacteria that control infection by Escovopsis in their fungal gardens. Although Atta spp. do not maintain symbiosis with protective actinobacteria, the evidence suggests that these insects are colonized by bacterial microbiota that may play a role in their defense against pathogens. The potential role of the bacterial microbiome of Atta workers in enhancing host immunity remains unexplored. We evaluated multiple parameters of the individual immunity of Atta cephalotes (Linnaeus, 1758) workers, including hemocyte count, encapsulation response, and the antimicrobial activity of the hemolymph in the presence or absence of bacterial microbiota. Experiments were performed on ants reared under standard conditions as well as on ants previously exposed to the entomopathogenic fungus Metharrizium anisopliae. Furthermore, the effects of the presence/absence of bacteria on the survival of workers exposed to M. anisopliae were evaluated. The bacterial microbiota associated with A. cephalotes workers does not modulate the number of hemocytes under control conditions or under conditions of exposure to the fungal pathogen. In addition, infection by M. anisopliae, but not microbiota, increases the encapsulation response. Similarly, the exposure of workers to this fungus led to increased hemolymph antimicrobial activity. Conversely, the removal of bacterial microbiota did not have a significant impact on the survival of workers with M. anisopliae. Our results suggest that the bacterial microbiota associated with the cuticle of A. cephalotes workers does not play a role as a modulator of innate immunity, either at baseline or after exposure to the entomopathogen M. anisopliae. Further, upon infection, workers rely on mechanisms of humoral immunity to respond to this threat. Overall, our findings indicate that the bacterial microbiota associated with A. cephalotes workers does not play a defensive role.