Gut microbiome composition is associated with spatial structuring and social interactions in semi-feral Welsh Mountain ponies

Abstract

Background: Microbiome composition is linked to host functional traits including metabolism and immune function. Drivers of microbiome composition are increasingly well-characterised; however, evidence of group-level microbiome convergence is limited and may represent a multi-level trait (i.e. across individuals and groups), whereby heritable phenotypes are influenced by social interactions. Here, we investigate the influence of spatial structuring and social interactions on the gut microbiome composition of Welsh mountain ponies.

Results: We show that semi-feral ponies exhibit variation in microbiome composition according to band (group) membership, in addition to considerable within-individual variation. Spatial structuring was also identified within bands, suggesting that despite communal living, social behaviours still influence microbiome composition. Indeed, we show that specific interactions (i.e. mother-offspring and stallion-mare) lead to more similar microbiomes, further supporting the notion that individuals influence the microbiome composition of one another and ultimately the group. Foals exhibited different microbiome composition to sub-adults and adults, most likely related to differences in diet.

Conclusions: We provide novel evidence that microbiome composition is structured at multiple levels within populations of social mammals and thus may form a unit on which selection can act. High levels of within-individual variation in microbiome composition, combined with the potential for social interactions to influence microbiome composition, suggest the direction of microbiome selection may be influenced by the individual members present in the group. Although the functional implications of this require further research, these results lend support to the idea that multi-level selection can act on microbiomes.

Keywords: 16S rRNA gene; Amplicon sequencing; Harem; Horizontal transmission; Life stage; Multi-level trait; Social networks; Spatial proximity; Vertical transmission.

Fig. 1

NMDS plot of the total microbiome of individual ponies in the study. Larger filled circles indicate the centroid for each individual

Fig. 2

Average (± SE) Jensen-Shannon divergence metrics for pony microbiome composition a within and between individuals; b within and between bands; c between mothers and their offspring, as well as between juveniles and non-maternal mares and foal-less mares; and d between the band stallion and band mares, and between all mares within a band. Significantly different results are indicated by *

Fig. 3

NMDS plots of the total microbiome of ponies plotted according to band membership (a) and life stage (b). Larger filled circles indicate group centroids

Fig. 4

a Map showing the spatial distribution of pony bands encountered during sampling. b Social network of the sampled individuals with edge width proportional to tie strength between individuals and c network visualisation of microbiome distance between individuals