Search bioRxiv⌕ Search

Biology subjects

Knowles, S. C.

Publications and source records attributed to Knowles, S. C..

5 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↗

Local density shapes complete brood failure across species boundaries in two sympatric songbirds

Reproduction in species with parental care involves sustaining a brood of offspring through an energetically demanding period, when shifts in resource availability, weather, predation risk, and parental condition can strongly alter offspring survival. The most extreme outcome is complete brood failure (death of all offspring), which is relatively frequent in many bird species and may occur when conditions cross a viability threshold. Although complete brood failure is important for shaping fitness variation and population dynamics, we have limited understanding of how intra- and interspecific density dependence governs these events, or of how factors such as habitat quality and disease burden contribute to them, because deriving this requires fine-scale, individual-level data collected across generations for multiple overlapping species. Using a dataset totalling 38,509 nesting attempts from great tits (Parus major) and blue tits (Cyanistes caeruleus) in Wytham Woods, Oxford, UK, we examined how brood failure is shaped by local conspecific and heterospecific density, habitat structure, and avian malaria infection for a subset. Complete brood failure was frequent (14.75%), mostly involving chick mortality in the nest consistent with starvation, rather than brood removal by predators. Relationships between density and brood failure were strong but species-specific. Specifically, great tit failure risk was higher in neighbourhoods that remained densely populated across years, whereas blue tit failure risk was lower where annual great tit or combined density was high, but not where annual blue tit density itself was high. This suggests that local overall density reflects continuing constraint for great tits, while local annual density may partly track favourable within-year conditions and settlement patterns for blue tits. In great tits, failure was also more common where oak density was low and farther from the closest river (Thames), while habitat associations were weak in blue tits. Malaria infection was spatially heterogeneous and covaried with density and habitat, but infection status did not significantly explain complete brood failure. Together, these results show that complete brood failure is shaped by spatially structured local ecological context, and how density dependence in these events can differ in direction and timescale between sympatric species.

ecology↗

Social and environmental transmission spread different sets of gut microbes in wild mice

Gut microbes shape many aspects of organismal biology, yet how these key bacteria transmit among hosts in natural populations remains poorly understood. Recent work in mammals has emphasized either transmission through social contacts or indirect transmission through environmental contact, but the relative importance of different routes has not been directly assessed. Here, we used a novel RFID-based tracking system to collect long-term high resolution data on social relationships, space use and microhabitat in a wild population of mice (Apodemus sylvaticus), while regularly characterising their gut microbiota. Through probabilistic modelling of the resulting data, we identify positive and statistically distinct signals of social and environmental transmission, captured by social networks and overlap in home ranges respectively. Strikingly, microbes with distinct biological attributes drove these different transmission signals. While aerotolerant spore-forming bacteria drove the effect of shared space use, a mix of taxa but especially anaerobic bacteria underpinned the social networks effect on gut microbiota similarity. These findings provide the first evidence for parallel social and environmental transmission of gut microbes that involve biologically distinct subsets of the mammalian gut microbiota. List of contributionsO_LIAura Raulo designed the study, helped develop the new RFID tracking technology, collected the data from Wytham, completed all laboratory analyses on gut microbiota profiling prior to sequencing, developed analytical methods, analysed the data and wrote the manuscript C_LIO_LIPaul Burkner helped design the Bayesian probabilistic modeling framework and provided feedback on the manuscript C_LIO_LIJarrah Dale helped collect field data using RFID loggers C_LIO_LIHolly English helped collect field data using RFID loggers and provided feedback on home range analyses C_LIO_LIGenevieve Finerty helped with home range analysis and the analysis of microhabitat variation and provided feedback on the manuscript C_LIO_LICurt Lamberth led development of RFID tracking devices and helped collect field data from Wytham C_LIO_LIJosh Firth supervised the research project, developed social network analysis methods and provided feedback on the analyses and the manuscript C_LIO_LITim Coulson supervised the research project and provided feedback on the analyses and the manuscript C_LIO_LISarah Knowles supervised the research project, helped develop the tracking technology and design the study, collected data from Wytham, planned and supervised laboratory methods, developed analytical methods and provided feedback on analyses and the manuscript. C_LI

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↗

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↗