Host-associated microbiomes play an increasingly appreciated role in animal metabolism, immunity and health. The microbes in turn depend on their host for resources and can be transmitted across the host’s social network. In this Perspective, we describe how animal social interactions and networks may provide channels for microbial transmission. We propose the ‘social microbiome’ as the microbial metacommunity of an animal social group. We then consider the various social and environmental forces that are likely to influence the social microbiome at multiple scales, including at the individual level, within social groups, between groups, within populations and species, and finally between species. Through our comprehensive discussion of the ways in which sociobiological and ecological factors may affect microbial transmission, we outline new research directions for the field.
Figure 1 – Social Microbiomes as Biological Archipelagos: Each island represents a host that is colonised by microbes, and in group-living species these hosts form ‘archipelagos’ for microbes. The central question is how the arrangement of islands affects microbial dispersal between them. Metacommunity theory and island biogeography theory can be applied to both sets of islands shown here. On the left is a representation of a spatially implicit model which ignores the effects of space, represented by islands that are evenly distributed to convey the idea that migration is equally likely between all islands (note that it is not possible to represent spatial distributions in the implicit model using two dimensions). This model does not account for the intrinsic social organisation of many animal species. In contrast, the social microbiome concept places social constraints on the organisation of host populations, yielding the island structure on the right (multiple, spatially distinct archipelagos), consistent with the idea of a spatially explicit model.
Figure 2 – Processes at Different Scales Influencing the Social Microbiome. At each scale, processes can affect microbial dispersal and selection, both of which can affect microbiome structure and function within individual hosts. Levels 1 to 5 describe the effects of individual-, intragroup-, intergroup-, intraspecies-, and interspecies interactions on the social microbiome. Level 1 encompasses individual social interactions within a group. Level 2 describes group characteristics that influence Level 1 interactions. Level 3 considers interactions between social groups of conspecifics. Level 4 captures differences between populations or species and the effects of the physical environment. Level 5 describes interactions between host species that inhabit the same physical environment. All levels are hypothesised to influence the microbial metacommunity of a host social group.
Figure 3 - Effect of Immigration on the Social Microbiome: Here, we show two hypothetical meerkat mobs, with the orange and blue ovals representing two distinct social microbiomes. Within each mob, there is a dominant female (represented by the largest animal in each group). There are also smaller subgroups of individuals that may interact more frequently with one another, and collectively engage in rearing the dominant female’s offspring. The group in between the two mobs represents a coalition migrating from the orange mob to the neighbouring blue mob (indicated by the orange-blue shaded arrow next to the group). During assimilation into the new mob, the migrants’ microbial composition is expected to change as a result of microbial transmission via social interactions with the new group. In addition, we predict that as the number of migrating individuals increases, so does the effect on the social microbiomes of both the natal group (right hand side, lower graph) and the receiving group (right hand side, lower graph).