Anthelmintic drugs modulate the acute phase immune response but not the microbiota in wild Song Sparrows

ABSTRACT Co-infection with microparasites (e.g., bacteria) and macroparasites (e.g., helminths) is often the natural state for wild animals. Despite evidence that gut helminths can bias immune responses away from inflammatory processes, few field studies have examined the role that helminths, or their potential interactions with internal microbial communities, play in modulating immunity in free-living, wild birds. Here, we used anthelmintic drugs to treat wild Song Sparrows (Melospiza melodia) for helminth infections and measured markers of systemic inflammation (heterothermia and locomotor activity) in response to an immune challenge with lipopolysaccharide (LPS), a cell wall component of gram-negative bacteria. Using birds from a population that previously showed high helminth prevalence, we monitored skin temperature and activity remotely using automated radio telemetry. We also collected cloacal swabs to determine whether drug treatment was associated with changes in the cloacal microbiota, and whether cloacal microbial community structure was associated with the severity of birds' immune responses. Because helminths can reduce the severity of inflammatory immune responses in other species, we predicted that in comparison with untreated control birds, anthelmintic-treated birds would be more lethargic and display higher fevers when challenged with LPS. Consistent with these predictions, anthelmintic-treated birds expressed higher fevers in response to immune challenge. However, all LPS-challenged birds decreased locomotor activity to a similar degree, regardless of anthelmintic treatment. Although several individual indicator bacterial taxa were strongly associated with anthelmintic treatment, this treatment did not alter overall bacterial alpha- and beta- diversity. Similarly, we did not find evidence that bacterial community diversity influenced the severity of immune responses to LPS. These results suggest that under field conditions, natural helminth infection can reduce the severity of songbirds' thermoregulatory responses (fever) during an immune challenge, without major impacts on internal microbial communities or behavioral responses to infection. LAY SUMMARY We treated wild Song Sparrows with de-worming drugs to determine how intestinal worms alter host immune responses and gut microbial diversity. In some mammals and domestic birds, intestinal worms can reduce immune responses to bacterial pathogens and alter diversity in gut microbial communities. However, we know little about such co-infection dynamics in wild birds. To probe these relationships, we treated wild, free-living Song Sparrows with de-worming drugs and injected them with endotoxin, a common bacterial molecule that activates the avian immune system. We used automated radio telemetry to measure immune responses (fever and reduced movement) and collected cloacal swabs to characterize gut microbes. Although we found no relationship between de-worming and movement or gut microbial diversity, de-wormed sparrows showed higher fevers after endotoxin treatment. These results suggest that in wild birds, co-infection with intestinal worms can alter some aspects of anti-bacterial immune defense, without major impacts on gut microbial symbioses.