The social side of symbionts: examining bidirectional links between the gut microbiome and social behaviour in mammals

Project Details

Key Questions

What role do gut microbes play in social communication among mice? Do microbial signals in faeces convey useful social information, for example about social group membership or suitability as a potential mate? Is naturally occurring individual variation in social behaviour shaped by the gut microbiome? How does social behaviour affect the transmission of gut-dwelling symbionts, that may be either beneficial or pathogenic? What behaviours might maximise the benefits relative to the costs of social interaction, in terms of symbiont transmission?

Background

Symbiotic microbial communities can have pervasive impacts on the biology of their hosts, and the diverse microbiomes that reside in the mammalian gut are no exception. Besides key roles in nutrition and pathogen defence, recent work has implicated the mammalian gut microbiome in shaping host behaviour. Of particular interest, the gut microbiome can affect mammalian social behaviour in various ways, including the modulation of scent-based social signals in species like hyenas, and through various physiological pathways collectively known as the microbiome-gut-brain axis. What’s more, links between the gut microbiome and social behaviour are likely to operate in both directions, with a growing body of research showing how social contacts and resulting transmission networks play an important role in shaping individual microbiomes. However, many gaps remain in our fundamental understanding of how gut microbes shape mammalian social behaviour and vice versa. While model systems like mice are revealing key mechanisms by which gut microbes can influence social behaviour under laboratory conditions, how these might play out in natural populations where microbiomes and host social interactions are far more variable, remains unknown. As such, there is much still to be discovered about the ecological and evolutionary significance of microbiome-behaviour interactions.

Aims of the Project

The aim of this project is to explore how the mammalian gut microbiome shapes and is shaped by social behaviour, using house mice as a model system.

Project Description

This project will combine investigation of wild house mice in a completely natural environment with controlled experiments in laboratory mice that take full advantage of their model organism status to derive causal insights about microbiome-behaviour links. For the wild mouse component, this project will use a wild mouse population that has been the subject of regular monitoring and individual gut microbiome profiling since 2019 as part of a large ERC-funded project https://www.knowleslab.com/study-systems/skokholm/. The mice of Skokholm represent a tractable wild system for which rich data on individuals' gut microbiome, social and genetic relationships is available.

The specific aims of this DPhil project would be finalized in discussion with the student, but several potential aims are listed below:

1. To examine the role of faecal microbial (scent) signals in communicating social information of relevance in natural populations, e.g. about social group, sex, and breeding partner suitability.

2. To investigate whether natural variation in social behaviour among wild individuals is influenced by their gut microbiome, and if so which microbes might be involved. This could be addressed by assaying social behaviour in wild mice, then using microbiome transplant experiments with germ-free mice to test whether social traits are transferred with the microbiome.

3. To investigate how social behaviour among wild mice influence the acquisition of both beneficial gut microbes and potential pathogens, and thus explore how organisms may trade-off the benefits and costs of social interaction in terms of symbiont transmission. This would involve analysis of wild mouse social network data collected using RFID technology over recent years, together with parallel data on their microbiomes and pathogenic infections diagnosed from faecal samples.

Methods to be used

The project is anticipated to use the following methods: (i) controlled experiments in laboratory mice (e.g. simple behavioural tests that explore the propensity of animals to provide and respond to social stimuli) (ii) microbiome transplant experiments using germ-free laboratory mice (iii) fieldwork to sample and collect behavioural data from wild mice (iv) molecular work to characterise microbiomes and pathogenic infections (v) computational analyses of detailed observational data from wild mice (e.g. social network analyses to explore relationships between social behaviour and symbiont transmission). Dr Knowles will support the design and implementation of animal experiments, fieldwork, molecular work to characterise faecal microbiomes and infections, and statistical analyses. Dr Firth will provide mentoring in data handling and statistical analyses of social network data from wild populations in the context of symbiont transmission, and Dr Green will support the design and analyses of experiments investigating mouse behaviour and communication.

Specialised skills required

A willingness to work with mice is essential for this project, and experience working with small animals would be highly advantageous. No other specialized skills are required. Experience handling and analysing large datasets in the R programming environment, and fieldwork experience would be beneficial.

Please contact Sarah Knowles on sarah.knowles@biology.ox.ac.uk if you are interested in this project