Temporal Stability and the Effect of Transgenerational Transfer on Fecal Microbiota Structure in a Long Distance Migratory Bird

Abstract

Animal bodies are inhabited by a taxonomically and functionally diverse community of symbiotic and commensal microorganisms. From an ecological and evolutionary perspective, inter-individual variation in host-associated microbiota contributes to physiological and immune system variation. As such, host-associated microbiota may be considered an integral part of the host’s phenotype, serving as a substrate for natural selection. This assumes that host-associated microbiota exhibits high temporal stability, however, and that its composition is shaped by trans-generational transfer or heritable host-associated microbiota modulators encoded by the host genome. Although this concept is widely accepted, its crucial assumptions have rarely been tested in wild vertebrate populations. We performed 16S rRNA metabarcoding on an extensive set of fecal microbiota (FM) samples from an insectivorous, long-distance migratory bird, the barn swallow (Hirundo rustica). Our data revealed clear differences in FM among juveniles and adults as regards taxonomic and functional composition, diversity and co-occurrence network complexity. Multiple FM samples from the same juvenile or adult collected within single breeding seasons exhibited higher similarity than expected by chance, as did adult FM samples over two consecutive years. Despite low effect sizes for FM stability over time at the community level, we identified an adult FM subset with relative abundances exhibiting significant temporal consistency, possibly inducing long-term effects on the host phenotype. Our data also indicate a slight maternal (but not paternal) effect on FM composition in social offspring, though this is unlikely to persist into adulthood. We discuss our findings in the context of both evolution and ecology of microbiota vs. host interactions and barn swallow biology.

Cloacal microbiota of barn swallows from Northern Italy

“…The phyla Proteobacteria, Actinobacteria, Firmicutes and Bacteroidetes dominated barn swallow CMs, consistently with the results on populations from the Czech Republic, which are~580 km far from our study area, where a high abundance of the phylum Tenericutes was also reported (Kreisinger et al 2015(Kreisinger et al , 2017. Proteobacteria and Firmicutes are common in the gastrointestinal trait of birds (Godoy-Vitorino et al 2012;Waite et al 2012;Waite & Taylor 2015).…”

“…Proteobacteria and Firmicutes are common in the gastrointestinal trait of birds (Godoy-Vitorino et al 2012;Waite et al 2012;Waite & Taylor 2015). A more detailed description of the bacterial community at a lower taxonomic level showed that the most abundant genera differed from those observed in previous studies: the genera Ralstonia, Pseudomonas, Aeribacillus, and Arenimonas were abundant in our samples, while they were not found in the two previous studies in the Czech Republic (Kreisinger et al 2015(Kreisinger et al , 2017. Ralstonia spp.…”

“…Interestingly, the two studies by Kreisinger and colleagues also found some differences in the CM compositions even among barn swallow populations that bred at short distance from one another. Indeed, in one paper (Kreisinger et al 2015), the most abundant genera were Candidatus Hamiltonella, Corynebacterium, Acinetobacter, and Comamonas, while in the other one (Kreisinger et al 2017), the most abundant genera were Mycoplasma, Catellicoccus, Serratia, Lactobacillus, and Dysgonomonas, together with some members of the family Enterobacteriaceae that were not classified at genus level. These differences may be due, at least partly, to the different methods used in the two studies.…”

“…These differences may be due, at least partly, to the different methods used in the two studies. Indeed, Kreisinger et al (2015) collected CM by using swabs as in the present study, while Kreisinger et al (2017) collected faeces to investigate faecal microbiota. However, faecal microbiota is generally considered as a proxy of bacterial communities of the lower intestine (Lewis et al 2016).…”

“…To date, only two published studies from the Czech Republic have investigated barn swallow CM (Kreisinger et al 2015(Kreisinger et al , 2017. In light of the large variability in the microbiota of bird populations from different geographical areas (Colston & Jackson 2016), our aim was to provide a description of the CM of a geographically different population.…”