Using fish models to investigate the links between microbiome and social behaviour: the next step for translational microbiome research?

Recent research has revealed surprisingly important connections between animals’ microbiome and social behaviour. Social interactions can affect the composition and function of the microbiome; conversely, the microbiome affects social communication by influencing the hosts’ central nervous system and peripheral chemical communication. These discoveries set the stage for novel research focusing on the evolution and physiology of animal social behaviour in relation to microbial transmission strategies. Here, we discuss the emerging roles of teleost fish models and their potential for advancing research fields, linked to sociality and microbial regulation. We argue that fish models, such as the zebrafish (Danio rerio, Cyprinidae), sticklebacks (‎Gasterosteidae), guppies (Poeciliidae) and cleaner–client dyads (e.g., obligate cleaner fish from the Labridae and Gobiidae families and their visiting clientele), will provide valuable insights into the roles of microbiome in shaping social behaviour and vice versa, while also being of direct relevance to the food and ornamental fish trades. The diversity of fish behaviour warrants more interdisciplinary research, including microbiome studies, which should have a strong ecological (field‐derived) approach, together with laboratory‐based cognitive and neurobiological experimentation. The implications of such integrated approaches may be of translational relevance, opening new avenues for future investigation using fish models

Ecological, evolutionary, and behavioral determinants of gut microbiomes in Malagasy mammals

Mammalian gut microbial communities govern host development, metabolism, immune function, and physiology, through interactions that range from commensal and mutualistic to pathogenic. However, we know little about the relative contributions of vertical, horizontal, and environmental transmission to gut microbiome composition, despite its importance to host health. To address this knowledge gap, I integrated field-collected data, molecular analyses, and computational and statistical approaches to examine how social networks and proximity to other host species influence bacteria transmission and gut microbiome composition in the wild mammals inhabiting Kirindy Mitea Biosphere Reserve in western Madagascar. In Chapter 1, I estimated the impacts of multilevel social structure, individual demographic traits, diet, scent-marking, and habitat overlap on gut bacteria acquisition in a wild lemur population (Verreaux’s sifaka, Propithecus verreauxi). The gut microbiomes of wild sifaka clearly reflected their social group membership, and both grooming and scent-marking behaviors promote microbial exchange and within-host diversity. In Chapter 2, I extended this work by examining how sifaka social dynamics influenced gut microbial turnover within individual animals and social groups over the course of several years. Sifaka social groups harbored distinct gut microbial communities throughout the study period, and compositional changes in the microbiota of individual animals were influenced by the gain or loss of unique social partners and dispersal between groups. In Chapter 3, I assayed the gut microbial communities of six sympatric (i.e., co-occurring) mammal populations— three lemur and three non-primate species – and assessed evolutionary, dietary, and behavioral predictors of microbiome functionality and composition. The ecological relationships among mammalian gut microbiomes mirrored their hosts’ phylogeny, with the three lemur species clustering separately from the other mammal species. The predicted functionality of lemur microbiomes differentiated according to diet, and distantly-related terrestrial mammals exhibited overlapping microbial communities, suggesting that ground dwelling facilitates the indirect horizontal transmission of gut bacteria among sympatric wild mammals. Together, these findings demonstrate that patterns of gut microbiome composition in wild mammals are scale-dependent: host phylogeny, diet, and substrate use shape microbial variation among sympatric mammal taxa, while social groupings and social contacts constrain the horizontal transmission of gut bacteria within a single host populationEcology, Evolution and Behavio

sifaka_trimmed_phyloseq_markedonly_normalized_openref

Phyloseq object containing normalized OTU counts for sifaka of known identity only. Place in "data" folder before running analyses

beta_diversity_adonis

R script for PERMANOVA analyses

samseq_differential_abundance_across_groups

R script that tests for differential abundance of bacterial phyla, families, and genera among sifaka social groups

sifaka_allotus_phyloseq_openref

Phyloseq object containing raw OTU counts (but singletons are removed). Place in "data" folder before running analyses

network_duration_function_dyad

R script that creates a social network using census, focal, and scan data

sifaka_unifrac_weighted_marked_openref

Matrix of weighted Unifrac distances among microbiome samples. Place in "data" folder before running analyses

census_data

Place in "data" folder before running analyses

diet_analyses

R script that tests between-group and between-individual differences in diet