Timing matters: Impacts of host selection and social environment on gut microbiota vary over host ontogeny in estrildid finches

Background: The assembly of gut microbiota during early development is a critical process influencing the development and fitness of vertebrates. Nevertheless, the relative influence of transmission from the early social environment and host selection over the host ontogeny is still underinvestigated, particularly in avian species. We conducted heterospecific and conspecific fostering experiments in Zebra finches (Taeniopygia guttata) and Bengalese finches (Lonchura striata domestica) under controlled conditions and repeatedly sampled the faecal microbiota of individual birds over the first three months of life. We documented the development of the gut microbiota and characterised the relative impacts of the early social environment and host selection due to species-specific characteristics and individual genetic backgrounds across different ontogenetic stages, employing 16S ribosomal RNA gene sequencing. Results: The gut microbiota's taxonomic composition and community structure changed across ontogenetic stages, and juveniles had higher alpha diversity than adults. Furthermore, in the early developmental stages, the microbial communities of chicks raised by conspecific and heterospecific foster parents resembled those of foster families, underpinning the importance of the social environment. In later stages, the social environment still influenced the microbiota, albeit with the increased impact of host selection. Conclusions: Overall, we provided a baseline description of the developmental succession of gut microbiota in zebra finch and Bengalese finches, which is a necessary first step for understanding the impact of early gut microbiota on host fitness. Furthermore, for the first time in avian species, we showed that the relative strengths of the two forces sculpturing the assembly and maintenance of gut microbiota (i.e. host selection and dispersal from the social environment) change during development, with an increasing weight of host selection. This should be considered while planning the studies of experimental manipulation of early-life gut microbiota. Our findings will also open new windows to study the mechanistic basis of host selection.