Microbial environment shapes immune function and cloacal microbiota dynamics in zebra finches Taeniopygia guttata

Abstract

Background: The relevance of the host microbiota to host ecology and evolution is well acknowledged. However, the effect of the microbial environment on host immune function and host microbiota dynamics is understudied in terrestrial vertebrates. Using a novel experimental approach centered on the manipulation of the microbial environment of zebra finches Taeniopygia guttata, we carried out a study to investigate effects of the host’s microbial environment on: 1) constitutive immune function, 2) the resilience of the host cloacal microbiota; and 3) the degree to which immune function and host microbiota covary in microbial environments that differ in diversity. Results: We explored immune indices (hemagglutination, hemolysis, IgY levels and haptoglobin concentration) and host-associated microbiota (diversity and composition) in birds exposed to two experimental microbial environments differing in microbial diversity. According to our expectations, exposure to experimental microbial environments led to differences related to specific antibodies: IgY levels were elevated in the high diversity treatment, whereas we found no effects for the other immune indices. Furthermore, according to predictions, we found significantly increased richness of dominant OTUs for cloacal microbiota of birds of the high diversity compared with the low diversity group. In addition, cloacal microbiota of individual females approached their baseline state sooner in the low diversity environment than females in the high diversity environment. This result supported a direct phenotypically plastic response of host microbiota, and suggests that its resilience depends on environmental microbial diversity. Finally, immune indices and cloacal microbiota composition tend to covary within treatment groups, while at the same time, individuals exhibited consistent differences of immune indices and microbiota characteristics. Conclusion: We show that microbes in the surroundings of terrestrial vertebrates can influence immune function and host-associated microbiota dynamics over relatively short time scales. We suggest that covariation between immune indices and cloacal microbiota, in addition to large and consistent differences among individuals, provides potential for evolutionary adaptation. Ultimately, our study highlights that linking environmental and host microbiotas may help unravelling immunological variation within and potentially among species, and together these efforts will advance the integration of microbial ecology and ecological immunology.