Out of the stable: Social disruption and concurrent shifts in the feral mare (Equus caballus) fecal microbiota

Abstract

The disruption of animals' symbiotic bacterial communities (their microbiota) has been associated with myriad factors including changes to the diet, hormone levels, and various stressors. The maintenance of healthy bacterial communities may be especially challenging for social species as their microbiotas are also affected by group membership, social relationships, microbial transfer between individuals, and social stressors such as increased competition and rank maintenance. We investigated the effects of increased social instability, as determined by the number of group changes made by females, on the microbiota in free-living, feral horses (Equus caballus) on Shackleford Banks, a barrier island off the North Carolina coast. Females leaving their groups to join new ones had fecal microbial communities that were similarly diverse but compositionally different than those of females that did not change groups. Changing groups was also associated with the increased abundance of a several bacterial genera and families. These changes may be significant as horses are heavily dependent upon their microbial communities for nutrient absorption. Though we cannot identify the particular mechanism(s) driving these changes, to the best of our knowledge, ours is the first study to demonstrate an association between acute social perturbations and the microbiota in a free-ranging mammal.

Keywords: alpha diversity; beta diversity; feral horse; microbiome; microbiota; social disruption.

FIGURE 1

Group changing status of Shackleford Banks, NC mares was not associated with microbiota alpha diversity in terms of its richness (a), evenness (b), or phylogenetic diversity (c). Each point represents a single fecal sample; some mares produced multiple samples. Median alpha diversity for each metric is shown with a solid line, while upper and lower dashed lines represent the 75th and 25th quantiles, respectively.

FIGURE 2

Betadispersion estimates differed between Shackleford Banks, NC mares that changed social groups and those that did not in Bray–Curtis space (a) and unweighted UniFrac space (b) but not in weighted UniFrac space (c). Each point represents a single fecal sample; some mares produced multiple samples. Median alpha diversity for each metric is shown with a solid line, while upper and lower dashed lines represent the 75th and 25th quantiles, respectively.

FIGURE 3

Group changing behavior by Shackleford Banks, NC mares was associated with a shift in microbial community composition, as described by Bray–Curtis dissimilarities (a) and unweighted (b) and weighted UniFrac (c) distances. Each point represents a single fecal sample; some mares produced multiple samples. Stress values refer to the stress of the ordination solution and printed p‐values are derived from PERMANOVA analysis describing the contribution of group‐change status to microbiota variation (reported in Table 4).

FIGURE 4

Bacteria in the genus Blautia (Phylum: Firmicutes, Class: Clostridia) were present in 24 of 52 fecal samples collected from Shackleford Banks, NC mares. The bacteria were significantly less abundant in the feces of mares that changed groups than in the feces of those that did not (FDR‐corrected p < .05).