Independent effects of cestode infection and simulated bacterial challenge on gene expression and microbiota in a social insect

Animal immune systems exhibit distinct responses to different parasitic infections, often involving specific yet interconnected pathways. In both vertebrates and invertebrates these immune responses can be further modulated by symbionts such as the gut microbiome. In this study, we examine how the social ant Temnothorax nylanderi responds to infection by the tapeworm Anomotaenia brevis and to a simulated bacterial challenge using lipopolysaccharides (LPS) from gram-negative bacteria. Our experimental approach assesses both the individual and combined effects of these challenges on two key metrics: transcriptional activity in the fat body, an organ crucial for immune defence, and the composition of the gut microbiome. We observed significant immune responses to both the tapeworm infection and the simulated bacterial challenge, with tapeworm infection having a more pronounced impact. There was no evidence of an interaction between the two challenges in either gut microbiome composition or gene expression profiles. However, upon inspection of commonly differentially expressed genes, we demonstrate that the two different immune challenges cause opposing effects in gene expression. This suggests that the tapeworm may selectively suppress the host’s immune response against itself while allowing the host to defend against other pathogens. We identified involved immune pathways, such as the Toll pathway, involved in both basal and induced immune responses in this social insect. Overall, our findings demonstrate that the same immune genes can be activated by different types of pathogens, whose effects may not be synergistic and can even go in opposite directions.