Abstract

BackgroundMicrobiome 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.ResultsWe 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.ConclusionsWe 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.

Highlights

  • Microbiome composition is linked to host functional traits including metabolism and immune function

  • An adonis analysis showed pony ID had a significant effect on total microbiome composition (p < 0.001; Table 2), with 52.6% of the variation in the microbiome attributable to individual variation (Fig. 1)

  • Despite the large amount of microbiome variation explained by ID, within-individual samples had significantly lower Jensen-Shannon Divergence (JSD) values than between-individual samples (χ2 = 391.62, df = 1, p < 0.001) (Fig. 2a)

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Summary

Introduction

Microbiome composition is linked to host functional traits including metabolism and immune function. The concept of a holobiont remains a topic of debate [2, 3], Antwis et al Microbiome (2018) 6:207 range of host sites for both mammalian and nonmammalian taxa [6,7,8]. Many host species have a considerable 'core' microbiome that is stable with a body site across individuals, time, and space [13,14,15,16,17]. This core microbiome is thought to represent the heritable "house-keeping" component of the microbiome, while there is a flexible component to the microbiome that varies based on environmental influences [5]. There is significant temporal variation in microbiome composition between and within individuals of a given species [18, 19]

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