Microbial transmission in the social microbiome and host health and disease.

Although social interactions are known to drive pathogen transmission, the contributions of socially transmissible host-associated mutualists and commensals to host health and disease remain poorly explored. We use the concept of the social microbiome-the microbial metacommunity of a social network of hosts-to analyze the implications of social microbial transmission for host health and disease. We investigate the contributions of socially transmissible microbes to both eco-evolutionary microbiome community processes (colonization resistance, the evolution of virulence, and reactions to ecological disturbance) and microbial transmission-based processes (transmission of microbes with metabolic and immune effects, inter-specific transmission, transmission of antibiotic-resistant microbes, and transmission of viruses). We consider the implications of social microbial transmission for communicable and non-communicable diseases and evaluate the importance of a socially transmissible component underlying canonically non-communicable diseases. The social transmission of mutualists and commensals may play a significant, under-appreciated role in the social determinants of health and may act as a hidden force in social evolution.

Epigenetic age estimation of wild mice using faecal samples.

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 limit 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 laboratory-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 laboratory 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 laboratory mice (and consistently higher epigenetic age estimates as a result), even among the smallest, juvenile mice. This suggests wild and laboratory mice may display different CpG methylation levels from very early in life and indicates caution is needed when developing epigenetic clocks on laboratory animals and applying them in the wild.

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. Utilizing noninvasive faecal samples from a long-term wild rodent study, we characterized viral communities of three common European rodent species (Apodemus sylvaticus, A. flavicollis and Myodes 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 common virus families, Picornaviridae, show pronounced temporal changes in viral richness and evenness, 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.

Hair cortisol concentration in Siberian flying squirrels is unrelated to landscape and social factors.

Intact ecosystems are being lost or modified worldwide, and many animal species are now forced to live in altered landscapes. A large amount of scientific studies have focused on understanding direct effects of habitat alterations on species occurrence, abundance, breeding success, and other life history aspects. Much less attention has been placed on understanding how habitat alterations impact on the physiology of species, e.g., via elevated chronic stress when living in an altered landscape. Here, we quantify the effects of individual age and sex, as well as effects of landscape and social factors on chronic stress of an endangered forest specialist species, the Siberian flying squirrel Pteromys volans. We collected hair samples over 2 years from across 192 flying squirrels and quantified their chronic stress response via cortisol concentrations. We then ran statistical models to relate cortisol concentrations with landscape and social factors. We show that cortisol concentrations in flying squirrels are neither affected by habitat amount and connectivity, nor by the density of conspecifics in the area. We however found that cortisol concentration was higher in adults than in pups, and in males compared with females. Lack of an effect of environmental factors on cortisol concentrations may indicate low physiological sensitivity to alterations in the surrounding environment, possibly due to low densities of predators that could induce stress in the study area. Further research should focus on possible effects of varying predator densities, alone and in interaction with landscape features, in shaping chronic stress of this and other species.

Social behaviour and gut microbiota in red-bellied lemurs (Eulemur rubriventer): In search of the role of immunity in the evolution of sociality.

Vertebrate gut microbiota form a key component of immunity and a dynamic link between an individual and the ecosystem. Microbiota might play a role in social systems as well, because microbes are transmitted during social contact and can affect host behaviour. Combining methods from behavioural and molecular research, we describe the relationship between social dynamics and gut microbiota of a group-living cooperative species of primate, the red-bellied lemur (Eulemur rubriventer). Specifically, we ask whether patterns of social contact (group membership, group size, position in social network, individual sociality) are associated with patterns of gut microbial composition (diversity and similarity) between individuals and across time. Red-bellied lemurs were found to have gut microbiota with slight temporal fluctuations and strong social group-specific composition. Contrary to expectations, individual sociality was negatively associated with gut microbial diversity. However, position within the social network predicted gut microbial composition. These results emphasize the role of the social environment in determining the microbiota of adult animals. Since social transmission of gut microbiota has the potential to enhance immunity, microbiota might have played an escalating role in the evolution of sociality.

Genetics and developmental biology of cooperation.

Despite essential progress towards understanding the evolution of cooperative behaviour, we still lack detailed knowledge about its underlying molecular mechanisms, genetic basis, evolutionary dynamics and ontogeny. An international workshop "Genetics and Development of Cooperation," organized by the University of Bern (Switzerland), aimed at discussing the current progress in this research field and suggesting avenues for future research. This review uses the major themes of the meeting as a springboard to synthesize the concepts of genetic and nongenetic inheritance of cooperation, and to review a quantitative genetic framework that allows for the inclusion of indirect genetic effects. Furthermore, we argue that including nongenetic inheritance, such as transgenerational epigenetic effects, parental effects, ecological and cultural inheritance, provides a more nuanced view of the evolution of cooperation. We summarize those genes and molecular pathways in a range of species that seem promising candidates for mechanisms underlying cooperative behaviours. Concerning the neurobiological substrate of cooperation, we suggest three cognitive skills necessary for the ability to cooperate: (i) event memory, (ii) synchrony with others and (iii) responsiveness to others. Taking a closer look at the developmental trajectories that lead to the expression of cooperative behaviours, we discuss the dichotomy between early morphological specialization in social insects and more flexible behavioural specialization in cooperatively breeding vertebrates. Finally, we provide recommendations for which biological systems and species may be particularly suitable, which specific traits and parameters should be measured, what type of approaches should be followed, and which methods should be employed in studies of cooperation to better understand how cooperation evolves and manifests in nature.

SIR+ models: accounting for interaction-dependent disease susceptibility in the planning of public health interventions.

Avoiding physical contact is regarded as one of the safest and most advisable strategies to follow to reduce pathogen spread. The flip side of this approach is that a lack of social interactions may negatively affect other dimensions of health, like induction of immunosuppressive anxiety and depression or preventing interactions of importance with a diversity of microbes, which may be necessary to train our immune system or to maintain its normal levels of activity. These may in turn negatively affect a population's susceptibility to infection and the incidence of severe disease. We suggest that future pandemic modelling may benefit from relying on 'SIR+ models': epidemiological models extended to account for the benefits of social interactions that affect immune resilience. We develop an SIR+ model and discuss which specific interventions may be more effective in balancing the trade-off between minimizing pathogen spread and maximizing other interaction-dependent health benefits. Our SIR+ model reflects the idea that health is not just the mere absence of disease, but rather a state of physical, mental and social well-being that can also be dependent on the same social connections that allow pathogen spread, and the modelling of public health interventions for future pandemics should account for this multidimensionality.

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 radio-frequency identification-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 characterizing their gut microbiota with 16S ribosomal RNA profiling. 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, microorganisms with distinct biological attributes drove these different transmission signals. While the social network effect on microbiota was driven by anaerobic bacteria, the effect of shared space was most influenced by aerotolerant spore-forming bacteria. These findings support the prediction that social contact is important for the transfer of microorganisms with low oxygen tolerance, while those that can tolerate oxygen or form spores may be able to transmit indirectly through the environment. Overall, these results suggest social and environmental transmission routes can spread biologically distinct members of the mammalian gut microbiota.

Finding common connections.

Ecological associations among gut bacteria are largely consistent across hosts in a population of wild baboons.

The genome sequence of the wood mouse, Apodemus sylvaticus (Linnaeus, 1758).

We present a genome assembly from an individual male Apodemus sylvaticus (the wood mouse; Chordata; Mammalia; Rodentia; Muridae). The genome sequence is 2,889.8 megabases in span. Most of the assembly is scaffolded into 25 chromosomal pseudomolecules, including the X and Y sex chromosomes. The mitochondrial genome has also been assembled and is 16.31 kilobases in length.

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

BACKGROUND: The mammalian gut microbiota influences a wide array of phenotypes which are relevant to 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. RESULTS: 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 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 identify a candidate maternally-transmitted bacterial family in wood mice, the Muribaculaceae. CONCLUSION: Overall, our findings point to an ontogenetically shifting transmission landscape in wild mice, with a mother's influence on microbiota composition waning as offspring age, while the relative impact of social contacts grows.

What are patterns of rise and decline?

The notions of change, such as birth, death, growth, evolution and longevity, extend across reality, including biological, cultural and societal phenomena. Patterns of change describe how success and composition of every entity, from species to societies, vary across time. Languages develop into new languages, music and fashion continuously evolve, economies rise and decline, ecological and societal crises come and go. A common way to perceive and analyse change processes is through patterns of rise and decline, the ubiquitous, often distinctively unimodal trajectories describing life histories of various entities. These patterns come in different shapes and are measured according to varying definitions. Depending on how they are measured, patterns of rise and decline can reveal, emphasize, mask or obscure important dynamics in natural and cultural phenomena. Importantly, the variations of how dynamics are measured can be vast, making it impossible to directly compare patterns of rise and decline across fields of science. Standardized analysis of these patterns has the potential to uncover important but overlooked commonalities across natural phenomena and potentially help us catch the onset of dramatic shifts in entities' state, from catastrophic crashes in success to gradual emergence of new entities. We provide a framework for standardized recognizing, characterizing and comparing patterns of change by combining understanding of dynamics across fields of science. Our toolkit aims at enhancing understanding of the most general tendencies of change, through two complementary perspectives: dynamics of emergence and dynamics of success. We gather comparable cases and data from different research fields and summarize open research questions that can help us understand the universal principles, perception-biases and field-specific tendencies in patterns of rise and decline of entities in nature.

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 Bifidobacterium castoris, Bifidobacterium animalis and Bifodobacterium pseudolongum were detected in wild mice (Apodemus sylvaticus, Apodemus agrarius and Apodemus 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, including in vitro growth assays, suggested that mouse-derived B. castoris strains encoded an extensive arsenal of carbohydrate-active enzymes, including putative novel glycosyl hydrolases such as chitosanases, 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 scales.

Synchronous Seasonality in the Gut Microbiota of Wild Mouse Populations.

The gut microbiome performs many important functions in mammalian hosts, with community composition shaping its functional role. However, the factors that drive individual microbiota variation in wild animals and to what extent these are predictable or idiosyncratic across populations remains poorly understood. Here, we use a multi-population dataset from a common rodent species (the wood mouse, Apodemus sylvaticus), to test whether a consistent "core" gut microbiota is identifiable in this species, and to what extent the predictors of microbiota variation are consistent across populations. Between 2014 and 2018 we used capture-mark-recapture and 16S rRNA profiling to intensively monitor two wild wood mouse populations and their gut microbiota, as well as characterising the microbiota from a laboratory-housed colony of the same species. Although the microbiota was broadly similar at high taxonomic levels, the two wild populations did not share a single bacterial amplicon sequence variant (ASV), despite being only 50km apart. Meanwhile, the laboratory-housed colony shared many ASVs with one of the wild populations from which it is thought to have been founded decades ago. Despite not sharing any ASVs, the two wild populations shared a phylogenetically more similar microbiota than either did with the colony, and the factors predicting compositional variation in each wild population were remarkably similar. We identified a strong and consistent pattern of seasonal microbiota restructuring that occurred at both sites, in all years, and within individual mice. While the microbiota was highly individualised, some seasonal convergence occurred in late winter/early spring. These findings reveal highly repeatable seasonal gut microbiota dynamics in multiple populations of this species, despite different taxa being involved. This provides a platform for future work to understand the drivers and functional implications of such predictable seasonal microbiome restructuring, including whether it might provide the host with adaptive seasonal phenotypic plasticity.

Social networks strongly predict the gut microbiota of wild mice.

The mammalian gut teems with 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 underexplored. 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 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.

Identifying Microbiome-Mediated Behaviour in Wild Vertebrates.

Recent research in laboratory animals has illuminated how the vertebrate gut microbiome can have diverse and powerful effects on the brain and behaviour. However, the ecological relevance of this microbiome-gut-brain (MGB) axis outside the laboratory remains unexplored. Here we argue that understanding behavioural and cognitive effects of the gut microbiome in natural populations is an important goal for behavioural ecology that may shed light on the mechanisms and evolution of behavioural plasticity. We outline a toolkit of approaches that could be applied in this endeavour and argue that beyond collecting observational data on the microbiome and behaviour from free-living animals, the incorporation of manipulative approaches tailored to such systems will be a key next step to progress understanding in this area.

Associations between glucocorticoids and sociality across a continuum of vertebrate social behavior.

The causes and consequences of individual differences in animal behavior and stress physiology are increasingly studied in wild animals, yet the possibility that stress physiology underlies individual variation in social behavior has received less attention. In this review, we bring together these study areas and focus on understanding how the activity of the vertebrate neuroendocrine stress axis (HPA-axis) may underlie individual differences in social behavior in wild animals. We first describe a continuum of vertebrate social behaviors spanning from initial social tendencies (proactive behavior) to social behavior occurring in reproductive contexts (parental care, sexual pair-bonding) and lastly to social behavior occurring in nonreproductive contexts (nonsexual bonding, group-level cooperation). We then perform a qualitative review of existing literature to address the correlative and causal association between measures of HPA-axis activity (glucocorticoid levels or GCs) and each of these types of social behavior. As expected, elevated HPA-axis activity can inhibit social behavior associated with initial social tendencies (approaching conspecifics) and reproduction. However, elevated HPA-axis activity may also enhance more elaborate social behavior outside of reproductive contexts, such as alloparental care behavior. In addition, the effect of GCs on social behavior can depend upon the sociality of the stressor (cause of increase in GCs) and the severity of stress (extent of increase in GCs). Our review shows that the while the associations between stress responses and sociality are diverse, the role of HPA-axis activity behind social behavior may shift toward more facilitating and less inhibiting in more social species, providing insight into how stress physiology and social systems may co-evolve.