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Raulo, A.

Publications and source records attributed to Raulo, A..

12 recordsLinked to original sources

Interspecific social contacts spread gut microbiota in wild rodent communities

Background: The mammalian gut microbiota influences a wide array of host phenotypes and varies substantially among individuals. Among conspecifics, microbiota composition is strongly shaped by microbial transmission through social interactions, yet the extent to which such transmission also occurs across species boundaries remains poorly understood. Here, we combine high-resolution tracking data collected over more than 10 months with gut microbiota profiling to examine social associations, space use, and microbiota similarity among individuals of three sympatric rodent species - wood mice (Apodemus sylvaticus), yellow-necked mice (A. flavicollis) and bank voles (Myodes glareolus), in two woodlands. By integrating multi-species social networks and spatial overlap with individual microbiota data, we test how both conspecific and interspecific interactions shape gut microbiota composition. Results: At both study sites, social associations strongly predicted microbiota similarity among conspecific individuals, whereas spatial proximity consistently predicted microbiota similarity among interspecific pairs. In addition, social associations between mice of different species predicted microbiota similarity, although this effect was weaker than that observed within species and was asymmetric, with evidence for stronger microbial transmission from wood mice to yellow-necked mice than vice versa. By focusing on species-indicative bacterial taxa, we further show that wood mice with more social connections to yellow-necked mice harboured a greater richness of gut bacteria typical of yellow-necked mice. Conclusions: Together, these results demonstrate that individual-level social behaviour can influence gut microbial transmission across species boundaries, particularly among closely related species with overlapping ecological niches. Interspecific social interactions may therefore represent an underappreciated pathway for the acquisition of novel gut symbionts in multi-species communities.

ecology↗

Orchestrating Microbiome Analysis with Bioconductor

The expansion of microbiome research has led to the accumulation of interlinked datasets encompassing versatile taxonomic and functional assays. The analysis of increasingly large and heterogeneous multi-modal microbiome data would benefit from unified approaches supporting the design of modular data science workflows through interoperable methods. The Bioconductor project has recently developed an optimized statistical programming framework for multi-assay data integration. Building on this foundation, we introduce a community-developed open source ecosystem for microbiome data science. In contrast to the previous alternatives, the methodology is specifically designed to support joint analysis of hierarchical, interlinked, and heterogeneous multi-table datasets that are increasingly common in modern microbiome research. This data science ecosystem encompasses open data, methods, tutorials, and an active online community. These resources support standardized and reproducible data wrangling, joint analysis, and reporting. We have detailed the functionality and usage in the online book https://microbiome.github.io/OMA, which offers guidance for prospective users and contributors.

bioinformatics↗

Age-related changes in the gut microbiota of a long-lived seabird suggest divergence from mammalian models

Gut microbiota plays key roles in shaping host development, immunity, and physiology. The assembly of vertebrate gut microbiota during early life follows relatively predictable trajectories across several mammalian species, largely driven by maternal transmission routes. However, birds lack these transmission mechanisms due to their oviparity, potentially leading to different age-related microbiota patterns. Here, we investigate gut microbiota variation in Atlantic puffin (Fratercula arctica) chicks and adults across six British populations using 16S rRNA amplicon sequencing. We find that chick microbiotas show strong population-level structuring that disappears in adults, with spatial patterns particularly pronounced in anaerobic bacteria. Puffin microbiotas become increasingly individualised and aerotolerant with age, while taxonomic richness remains stable - patterns that contrast with the convergent, richness-increasing trajectories observed in several mammalian species. Our results suggest that environmental exposure drives early-life microbiota assembly in birds, highlighting the value of avian systems for understanding vertebrate microbiota development beyond mammals.

ecology↗

The gut microbiota of two rodents varies over fine spatial scales yet is minimally influenced by the environmental microbiota

The gut microbiota of animals varies considerably between individuals within the same population. Given the importance of gut microbiota composition for animal biology and ultimately fitness (e.g., via effects on physiology, immunity and even behaviour), there is considerable interest in understanding which factors shape its variation. Here, we tested whether local environments are an important source of microbial diversity for mammalian guts, by sampling the faecal microbiota of wood mice (Apodemus sylvaticus) and bank voles (Myodes glareolus), as well as environmental microbiotas, across Wytham Woods. We first find that both species share a low proportion of their microbiotas with local environments and that most shared microbes are aerotolerant. We then detect that microgeographic patterns (namely soil chemistry) are associated with variation in the microbiota of local environments but this does not translate to microbiota variation between animals. Nevertheless, between-individual gut microbiota variation is strongly associated with where animals are sampled, suggesting that other local factors (e.g., biotic environment, interactions between individuals) are much stronger predictors of microbiota composition than local abiotic factors. Finally, we find that wood mice (but not bank voles) are more likely to share microbes with local than non-local environments, but that local environments still contribute little to animal microbiotas. Our findings challenge the prevailing view that mammalian microbiotas are strongly affected by local soil chemistry or the abiotic environment, while further supporting the prediction that biotic and/or other intrinsic factors (which can also act on a local scale) contribute more to microbiota composition.

ecology↗

Habitat quality influences gut microbiota via cortisol in Siberian flying squirrels (Pteromys volans)

Inconspicuous interactions between host physiological systems and resident microbial communities may underlie how animals respond to environmental change. For example, immunity and metabolism are regulated in part by the gut microbiota, which can be shaped indirectly by host neuroendocrine function via a "gut-brain axis". Yet the sensitivity of this axis in wild vertebrates remains ambiguous. Here, we investigate covariation among environmental quality, glucocorticoids, and gut microbiota in a vulnerable population of Siberian flying squirrels (Pteromys volans) inhabiting a region impacted by variable rates of human disturbance. We test competing hypotheses related to direct versus indirect environmental effects (via the gut-brain axis) on adult and juvenile gut microbial communities. Adults housed a richer gut microbiota and had higher hair glucocorticoids that covaried with microbial composition, while juveniles lacked any hormone-microbiome covariation. Environmental quality (patch size, habitat diversity, and suitability) predicted variation in glucocorticoids but not variation in microbial diversity, suggesting no direct effects on gut microbiota. Instead, structural equation models revealed indirect environmental effects on microbiota via elevations in glucocorticoids in adults. Among juveniles, habitat-induced hormonal responses had no downstream effects on microbial diversity. Together, this provides evidence for age-dependent indirect environmental effects on gut microbial composition in a wild mammal by way of the host neuroendocrine system.

ecology↗

Territorial behavior as a route of social microbial transmission in an asocial mammal

Microbial transmission is a major benefit of sociality, facilitated by affiliative behaviors such as grooming and communal nesting in group-living animals. The spread of microbial symbionts through these pathways, and their incorporation into host microbiomes, can enhance host health and fitness by contributing to pathogen protection and metabolic flexibility. Are pathways that facilitate microbial transfer across hosts also present in animals that do not form social groups because territoriality limits social interactions and prevents group formation? Here, we addressed this question by combining longitudinal sampling of individual gut microbial communities, demographic data, and dynamic behavioral and spatial measures of territoriality from a non-social, highly territorial small mammal: wild North American red squirrels (Tamiasciurus hudsonicus). As squirrel densities increased, individual gut microbial communities became richer and more phylogenetically diverse, while among-individual differences in composition decreased. This pattern was characterized primarily by increases in obligately anaerobic and non-sporulating taxa with little to no tolerance for oxygen-rich environments, suggesting social rather than environmental routes of transmission. Moreover, territorial intrusions--in which conspecifics were found on within an individuals territorial space--increased gut microbial diversity among individuals defending larger territorial spaces. Using an intrusion-based social network analysis, we found that that pairs with stronger social association (via intrusions) exhibited higher gut microbial similarity. Taken together, our findings provide some of the first evidence for social microbial transmission in a non-social species, and suggest that increased density and territorial behavior can diversify and homogenize host gut microbial communities despite social isolation.

ecology↗

Elevated epigenetic age in wild compared to lab-raised house mice

Age is a key parameter in population ecology, with a myriad of biological processes changing with age as organisms develop in early life then later senesce. As age is often hard to accurately measure with non-lethal methods, epigenetic methods of age estimation (epigenetic clocks) have become a popular tool in animal ecology, and are often developed or calibrated using captive animals of known age. However, studies typically rely on invasive blood or tissue samples, which limits their application in more sensitive or elusive species. Moreover, few studies have directly assessed how methylation patterns and epigenetic age estimates compare across environmental contexts (e.g., captive or lab-based vs. wild animals). Here, we built a targeted epigenetic clock from laboratory house mice (strain C57BL/6, Mus musculus) using DNA from non-invasive faecal samples, and then used it to estimate age in a population of wild mice (Mus musculus domesticus) of unknown age. This lab mouse-derived epigenetic clock accurately predicted adult wild mice to be older than juveniles, and showed that wild mice typically increased in epigenetic age over time, but with wide variation in epigenetic ageing rate among individuals. Our results also suggested that, for a given body mass, wild mice had higher methylation across targeted CpG sites than lab mice (and consistently higher epigenetic age estimates as a result), even among the smallest, juvenile mice. This suggests wild and lab mice may display different CpG methylation levels from very early in life, and indicates caution is needed when developing epigenetic clocks on lab animals and applying them in the wild.

molecular biology↗

Early-life gut microbiota assembly patterns are conserved between laboratory and wild mice

Assembly of the mammalian gut microbiota during early life is known to shape key aspects of organismal development, including immunity, metabolism and behaviour. While house mice (Mus musculus) are the major laboratory model organism for gut microbiota research, their artificial lab-based lifestyle could fundamentally alter ecological processes of microbiota assembly and dynamics, in ways that affect their usefulness as a model system. To examine this, here we directly compared patterns of gut microbiota assembly in house mice from the lab and from the wild, making use of a tractable, individually-marked wild population where we could examine patterns of gut microbiota assembly during early life. Despite lab and wild mice harbouring taxonomically distinct communities, we identify striking similarities in multiple patterns of their gut microbiota assembly. Specifically, age-related changes in both alpha and beta diversity, as well as the abundance of predominant phyla and aerotolerance of the microbiota followed parallel trajectories in both settings. These results suggest some degree of intrinsic programme in gut microbiota assembly that transcends variation in taxonomic profiles, and the genetic and environmental background of the host. They further support the notion that despite their artificial environment, lab mice can provide meaningful insights into natural microbiota ecological dynamics in early life and their interplay with host development.

ecology↗

Maternal transmission gives way to social transmission during gut microbiota assembly in wild mice

The mammalian gut microbiota influences a wide array of phenotypes and is considered a key determinant of fitness, yet knowledge about the transmission routes by which gut microbes colonise hosts in natural populations remains limited. Here, we use an intensively studied wild population of wood mice (Apodemus sylvaticus) to examine how vertical (maternal) and horizontal (social) transmission routes influence gut microbiota composition throughout life. We identify independent signals of maternal transmission (sharing of taxa between a mother and her offspring) and social transmission (sharing of taxa predicted by the social network), whose relative magnitudes shift as hosts age. In early life, gut microbiota composition is predicted to a similar extent by both maternal and social relationships, but by adulthood the impact of maternal transmission becomes undetectable, leaving only a signal of social transmission. By exploring which taxa drive the maternal transmission signal, we further identify a candidate maternally-transmitted bacterial family in wood mice, the Lactobacillaceae. Overall, our findings suggest a shifting transmission landscape for wild mice, with a mothers influence on microbiota composition waning as offspring age, while the impact of social contacts remains strong and consistent.

microbiology↗

Seasonal dynamics of the wild rodent faecal virome

Viral discovery studies in wild animals often rely on cross-sectional surveys at a single time point. As a result, our understanding of the temporal stability of wild animal viromes remains poorly resolved. While studies of single host-virus systems indicate that host and environmental factors influence seasonal virus transmission dynamics, comparable insights for whole viral communities in multiple hosts are lacking. Leveraging non-invasive faecal samples from a long-term wild rodent study, we characterised viral communities of three common European rodent species (Apodemus sylvaticus, A. flavicollis, and M. glareolus) living in temperate woodland over a single year. Our findings indicate that a substantial fraction of the rodent virome is seasonally transient and associated with vertebrate or bacteria hosts. Further analyses of one of the most abundant virus families, Picornaviruses, show pronounced temporal changes in viral richness and diversity, which were associated with concurrent and up to [~]3-month lags in host density, ambient temperature, rainfall and humidity, suggesting complex feedbacks from the host and environmental factors on virus transmission and shedding in seasonal habitats. Overall, this study emphasizes the importance of understanding the seasonal dynamics of wild animal viromes in order to better predict and mitigate zoonotic risks.

ecology↗

Bifidobacterium castoris strains isolated from wild mice show evidence of frequent host switching and diverse carbohydrate metabolism potential

Members of the gut microbiota genus Bifidobacterium are widely distributed human and animal symbionts believed to exert beneficial effects on their hosts. However, in-depth genomic analyses of animal-associated species and strains are somewhat lacking, particularly in wild animal populations. Here, to examine patterns of host specificity and carbohydrate metabolism capacity, we sequenced whole genomes of Bifidobacterium isolated from wild-caught small mammals from two European countries (UK and Lithuania). Members of B. castoris, B. animalis and B. pseudolongum were detected in wild mice (Apodemus sylvaticus, A. agrarius and A. flavicollis), but not voles or shrews. B. castoris constituted the most commonly recovered Bifidobacterium (78% of all isolates), with the majority of strains only detected in a single population, although populations frequently harboured multiple co-circulating strains. Phylogenetic analysis revealed that the mouse-associated B. castoris clades were not specific to a particular location or host species, and their distribution across the host phylogeny was consistent with regular host shifts rather than host-microbe codiversification. Functional analysis suggested that mouse-derived B. castoris strains encoded an extensive arsenal of carbohydrate-active enzymes, including putative novel glycosyl hydrolases such as chitosanases that may act on chitin-derived substrates such as mushrooms or insects, along with genes encoding putative exopolysaccharides, some of which may have been acquired via horizontal gene transfer. Overall, these results provide a rare genome-level analysis of host specificity and genomic capacity among important gut symbionts of wild animals, and reveal that Bifidobacterium has a labile relationship with its host over evolutionary time scale.

microbiology↗

Social networks strongly predict the gut microbiota of wild mice

The mammalian gut teems with beneficial microbes, yet how hosts acquire these symbionts remains poorly understood. Research in primates suggests that microbes can be picked up via social contact, but the role of social interactions in non-group-living species remains unexplored. Here, we use a passive tracking system to collect high resolution spatiotemporal activity data from wild mice (Apodemus sylvaticus). Social network analysis revealed social association strength to be the strongest predictor of microbiota similarity among individuals, controlling for factors including spatial proximity and kinship, which had far smaller or nonsignificant effects. This social effect was limited to interactions involving males (male-male and male-female), implicating sex-dependent behaviours as driving processes. Social network position also predicted microbiota richness, with well-connected hub individuals having the most diverse microbiotas. Overall, these findings suggest social contact provides a key transmission pathway for gut symbionts even in relatively asocial mammals, that strongly shapes the adult gut microbiota. This work underlines the potential for individuals to pick up beneficial symbionts as well as pathogens from social interactions.

ecology↗