Ectoparasitism and the gut microbiota: a cross-fostering experiment in a wild passerine

The gut microbiota plays a key role in host development, physiology, and immunity, and is likely shaped by hosts' genetic and environmental factors, including ectoparasitism and, thus, host health. Here, we experimentally manipulated ectoparasite (Carnus hemapterus) abundance in spotless starling (Sturnus unicolor) nests. We evaluated its hypothesized disruptive effects on nestling gut microbiota and explored also whether the effects depend on sibling relatedness using a partial cross-fostering design. Experimentally increased parasitism significantly affected alpha but not beta diversity of the bacterial community in 14-day-old cross-fostered nestlings, i.e. those non-genetically related to their social parents and siblings. The experimental parasite manipulation also affected the relative abundance of 123 bacterial strains, including fermenters, mucosa-adapted bacterial symbionts, and opportunistic pathogens. Finally, gut microbiota composition was also associated with nestling phenotype (body mass, wing and tarsus length, carotenoid concentration, and telomere dynamics). Sparse PLS network analyses linked body mass (positively: Erysipelatoclostridium, Parabacteroides, and Helicobacter; negatively: Salmonella) and parasitism intensity (negatively: Dubosiella, Rickettsiella, and Helicobacter) with relative abundance of specific bacterial strains. These results provide the first evidence in natural conditions that the effects of ectoparasites on gut microbiota depend on genetic relatedness between nestlings and parents, highlighting the complex interplay between parasitism, microbiota, and host traits.