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.
Highlights
The bodies of animals are inhabited by taxonomically and functionally diverse communities of symbiotic and commensal microorganisms (Qin et al, 2010; Muegge et al, 2011)
Coverage indices calculated for individual samples indicated that our data captured the vast majority of fecal microbiota (FM) diversity
Barn swallow FM was dominated by Proteobacteria, Firmicutes (34.7 ± 1.4%, range = 13.2– 99.1%), Tenericutes (12.7 ± 1.1%, range = 0–96.0%), Bacteroidetes (6.3 ± 0.7%, range = 0–92.2%), and Actinobacteria (4.4 ± 0.4%, range = 0–48.7%), with other phyla present at much lower frequencies
Summary
The bodies of animals are inhabited by taxonomically and functionally diverse communities of symbiotic and commensal microorganisms (Qin et al, 2010; Muegge et al, 2011) Recent advances in this field have clearly shown that such host-associated microbiota provide important benefits to the host. Unlike host-encoded enzymes, enzymes encoded by the microbial metagenome enable cleavage of complex substrates such as plant polysaccharides Products of these pathways can be further processed by the host’s metabolism and, microbial communities positively contribute to the host’s energy balance (Jumpertz et al, 2011). In addition to these benefits, certain species of host-associated microbiota can induce harmful effects, such as reduced diet processing capacity (Smith et al, 2013), chronic inflammation (Dapito et al, 2012), or production of toxins (Yoshimoto et al, 2013)
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