Friend or foe? Effects of host immune activation on the gut microbiome in the caterpillar Manduca sexta

For many animals, the gut microbiome plays an essential role in immunity and digestion. However, certain animals, such as the caterpillar Manduca sexta, do not have a resident gut microbiome. Although these animals do have bacteria that pass through their gut from their natural environment, the absence of such bacteria does not reduce growth or survival. We hypothesized that M. sexta would sterilize their gut as a protective measure against secondary infection when faced with a gut infection or exposure to heat-killed bacteria in the blood (haemolymph). However, we found that gut sterilization did not occur during either type of immune challenge, i.e. bacterial numbers did not decrease. By examining the pattern of immune-related gene expression, gut pH, live bacterial counts and mass change (as a measure of sickness behaviour), we found evidence for physiological trade-offs between regulating the microbiome and defending against systemic infections. Caterpillars exposed to both gut pathogens and a systemic immune challenge had higher numbers of bacteria in their gut than caterpillars exposed to a single challenge. Following a multivariate analysis of variance, we found that the response patterns following an oral challenge, systemic challenge or dual challenge were unique. Our results suggest that the immune response for each challenge resulted in a different configuration of the immunophysiological network. We hypothesize that these different configurations represent different resolutions of physiological tradeoffs based on the immune responses needed to best protect the animal against the present immune challenges.