Timing matters: age-dependent impacts of the social environment and host selection on the avian gut microbiota

Background The establishment of the gut microbiota in early life is a critical process that influences the development and fitness of vertebrates. However, the relative influence of transmission from the early social environment and host selection throughout host ontogeny remains understudied, particularly in avian species. We conducted conspecific and heterospecific cross-fostering experiments in zebra finches (Taeniopygia guttata) and Bengalese finches (Lonchura striata domestica) under controlled conditions and repeatedly sampled the faecal microbiota of these birds over the first 3 months of life. We thus 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 ontogeny by using 16S ribosomal RNA gene sequencing. Results The taxonomic composition and community structure of the gut microbiota changed across ontogenetic stages; juvenile zebra finches exhibited higher alpha diversity than adults at the post-breeding stage. Furthermore, in early development, the microbial communities of juveniles raised by conspecific and heterospecific foster parents resembled those of their foster family, emphasising the importance of the social environment. In later stages, the social environment continued to influence the gut microbiota, but host selection increased in importance. Conclusions We provided a baseline description of the developmental succession of gut microbiota in zebra finches and Bengalese finches, which is a necessary first step for understanding the impact of the early gut microbiota on host fitness. Furthermore, for the first time in avian species, we showed that the relative strengths of the two forces that shape the establishment and maintenance of the gut microbiota (i.e. host selection and dispersal from the social environment) change during development, with host selection increasing in importance. This finding should be considered when experimentally manipulating the early-life gut microbiota. Our findings also provide new insights into the mechanisms of host selection

Bats, Bacteria, and Bat Smell V.2.0: Repeatable Sex-Specific Differences in Scent Organ Microbiota

Maraci Ö, Antonatou-Papaioannou A, Jünemann S, et al. Bats, Bacteria, and Bat Smell V.2.0: Repeatable Sex-Specific Differences in Scent Organ Microbiota. Microbial Ecology . 2024;87(1): 55.Reproducibility is a fundamental principle in science, ensuring reliable and valid findings. However, replication studies are scarce, particularly in ecology, due to the emphasis on novelty for publication. We explored the possibility of replicating original findings in the field of microbial and chemical ecology by conducting a conceptual replication of a previous study analysing the sex-specific differences in the microbial communities inhabiting the wing sacs, a scent organ with crucial functions in olfactory communication, of greater sac-winged bat (Saccopteryx bilineata). In the original study, the skin swabs from the antebrachial wing sacs of the males and wing sac rudiments of the females were analysed using culture-dependent methods to test sex-specific differences. The authors demonstrated that males have lower microbial richness and different microbial composition than females. We attempted to reproduce these findings using 16S rRNA sequencing, which offers improved accuracy in pinpointing microbial members than culture-dependent methods because of advanced statistical methods. Our study validated the original study's findings: Males had a lower microbial richness, and the community composition differed between the sexes. Furthermore, in the current study, males had an increased abundance of bacteria that might potentially be involved in odour production and degradation of malodorous substances and antimicrobial production. Our conceptual replication study corroborated that microbes can play a role in shaping their host's olfactory phenotype and consequently influence sexual selection. Furthermore, the current study emphasises the importance of replication efforts and hopefully encourages a culture that values replication studies in scientific practice. © 2024. The Author(s)

The Gut Microbial Composition Is Species-Specific and Individual-Specific in Two Species of Estrildid Finches, the Bengalese Finch and the Zebra Finch

Maraci Ö, Antonatou-Papaioannou A, Jünemann S, et al. The Gut Microbial Composition Is Species-Specific and Individual-Specific in Two Species of Estrildid Finches, the Bengalese Finch and the Zebra Finch. Frontiers in Microbiology. 2021;12: 619141.Microbial communities residing in the gastrointestinal tracts of animals have profound impacts on the physiological processes of their hosts. In humans, host-specific and environmental factors likely interact together to shape gut microbial communities, resulting in remarkable inter-individual differences. However, we still lack a full understanding of to what extent microbes are individual-specific and controlled by host-specific factors across different animal taxa. Here, we document the gut microbial characteristics in two estrildid finch species, the Bengalese finch (Lonchura striata domestica) and the zebra finch (Taeniopygia guttata) to investigate between-species and within-species differences. We collected fecal samples from breeding pairs that were housed under strictly controlled environmental and dietary conditions. All individuals were sampled at five different time points over a range of 120 days covering different stages of the reproductive cycle. We found significant species-specific differences in gut microbial assemblages. Over a period of 3 months, individuals exhibited unique, individual-specific microbial profiles. Although we found a strong individual signature in both sexes, within-individual variation in microbial communities was larger in males of both species. Furthermore, breeding pairs had more similar microbial profiles, compared to randomly chosen males and females. Our study conclusively shows that host-specific factors contribute structuring of gut microbiota

Alterations to the Gut Microbiota of a Wild Juvenile Passerine in an Urban Mosaic

Maraci Ö, Corsini M, Antonatou-Papaioannou A, et al. Alterations to the Gut Microbiota of a Wild Juvenile Passerine in an Urban Mosaic. bioRxiv. 2021.**Abstract** Urbanisation is a major anthropogenic perturbation that progressively alters multiple environmental parameters, thereby presenting novel evolutionary challenges to wild populations. Symbiotic microorganisms residing in the gastrointestinal tracts (gut) of vertebrates have well-established mutual connections with the physiology of their hosts and respond quickly to environmental alterations. However, the impacts of anthropogenic changes and urbanisation on gut microbiota remain poorly understood, especially in early development. To address this knowledge gap, we investigated the gut microbiota in juvenile great tits (Parus major) in an urban mosaic. First, we compared the microbiota of nestlings reared in artificial nest boxes or natural cavities. Next, we analysed microbiota variations employing two distinct urbanisation frameworks, (i) the classical urban/rural dichotomy and (ii) gradual changes in the amount of impervious surface area (ISA) in the urban space and identified the environmental variables that predicted the changes in the microbial communities. Alpha diversity was influenced by cavity type and by the amount of impervious surface surrounding the breeding location. Alpha diversity was also positively correlated with the tree cover density. Beta diversity differed between urban and rural sites, and these alterations covaried with sound pollution, the distance to the city centre and the distance to the closest road. Overall, the microbial communities reflect and are possibly influenced by the heterogeneous environmental modifications that are typical of the urban space. Strikingly, the choice of framework used to define the urban space can influence the outcomes of studies investigating animal-microbe symbiosis. Our results open new perspectives from which the potential function of microbial symbionts in the adaptation of their hosts to anthropogenic stress can be investigated

Changes to the gut microbiota of a wild juvenile passerine in a multidimensional urban mosaic

Maraci Ö, Corsini M, Antonatou-Papaioannou A, et al. Changes to the gut microbiota of a wild juvenile passerine in a multidimensional urban mosaic. Scientific Reports. 2022;12(1): 6872.Urbanisation is a major anthropogenic perturbation presenting novel ecological and evolutionary challenges to wild populations. Symbiotic microorganisms residing in the gastrointestinal tracts (gut) of vertebrates have mutual connections with host physiology and respond quickly to environmental alterations. However, the impact of anthropogenic changes and urbanisation on the gut microbiota remains poorly understood, especially in early development. To address this knowledge gap, we characterised the gut microbiota of juvenile great tits (Parus major) reared in artificial nestboxes and in natural cavities in an urban mosaic, employing two distinct frameworks characterising the urban space. Microbial diversity was influenced by cavity type. Alpha diversity was affected by the amount of impervious surface surrounding the breeding location, and positively correlated with tree cover density. Community composition differed between urban and rural sites: these alterations covaried with sound pollution and distance to the city centre. Overall, the microbial communities reflect and are possibly influenced by the heterogeneous environmental modifications that are typical of the urban space. Strikingly, the choice of framework and environmental variables characterising the urban space can influence the outcomes of such ecological studies. Our results open new perspectives to investigate the impact of microbial symbionts on the adaptive capacity of their hosts. © 2022. The Author(s)

Timing matters: Age-dependent impacts of the social environment and host selection on the avian gut microbiota

Maraci Ö, Antonatou-Papaioannou A, Jünemann S, et al. Timing matters: Age-dependent impacts of the social environment and host selection on the avian gut microbiota. 2022.**Abstract**Background:The establishment of the gut microbiota in early life is a critical process that influences the development and fitness of vertebrates. However, the relative influence of transmission from the early social environment and host selection throughout host ontogeny remains understudied, particularly in avian species. We conducted conspecific and heterospecific cross-fostering experiments in zebra finches (Taeniopygia guttata) and Bengalese finches (Lonchura striata domestica) under controlled conditions and repeatedly sampled the faecal microbiota of these birds over the first three months of life. We thus 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 ontogeny by using 16S ribosomal RNA gene sequencing.Results:The taxonomic composition and community structure of the gut microbiota changed across ontogenetic stages; juveniles exhibited higher alpha diversity than adults. Furthermore, in early development, the microbial communities of juveniles raised by conspecific and heterospecific foster parents resembled those of their foster family, emphasizing the importance of the social environment. In later stages, the social environment continued to influence the gut microbiota, but host selection increased in importance.Conclusions:We provided a baseline description of the developmental succession of gut microbiota in zebra finches and Bengalese finches, which is a necessary first step for understanding the impact of the early gut microbiota on host fitness. Furthermore, for the first time in avian species, we showed that the relative strengths of the two forces that shape the establishment and maintenance of the gut microbiota (i.e.,host selection and dispersal from the social environment) change during development, with host selection increasing in importance. This finding should be considered when experimentally manipulating the early-life gut microbiota. Our findings also provide new insights into the mechanisms of host selection