Seasonal dynamics in the mammalian microbiome between disparate environments

Abstract

Host-associated bacterial microbiomes can facilitate host acclimation to seasonal environmental change and are hypothesized to help hosts cope with recent anthropogenic environmental perturbations (e.g., landscape modification). However, it is unclear how recurrent and recent forms of environmental change interact to shape variation in the microbiome. The majority of wildlife microbiome research occurs within a single seasonal context. Meanwhile, the few studies of seasonal variation in the microbiome often restrict focus to a single environmental context. By sampling urban and exurban eastern grey squirrel populations in the spring, summer, autumn, and winter, we explored whether seasonal rhythms in the grey squirrel gut microbiome differed across environments using a 16S amplicon sequencing approach. Differences in the microbiome between urban and exurban squirrels persisted across most of the year, which we hypothesize is linked to anthropogenic food consumption, but we also observed similarities in the urban and exurban grey squirrel microbiome during the autumn, which we attribute to engrained seed caching instincts in preparation for the winter. Host behaviour and diet selection may therefore be capable of maintaining similarities in microbiome structure between disparate environments. However, the depletion of an obligate host mucin glycan specialist (Akkermansia) during the winter in both urban and exurban squirrels was among the strongest differential abundance patterns we observed. In summary, urban grey squirrels showed different seasonal patterns in their microbiome than squirrels from exurban forests; however, in some instances, host behaviour and physiological responses might be capable of maintaining similar microbiome responses across seasons.

Keywords: 16S amplicon; bacteria; grey squirrel; gut; landscape modification; urban; wildlife.

FIGURE 1

(a) Principal coordinate plot of Bray–Curtis dissimilarities in the eastern grey squirrel faecal microbiome, with the first and second principal coordinates of ordinations visualized in boxplots separated by season and environment and (b) a hierarchical clustering plot of Bray–Curtis dissimilarities from rarefied samples pooled by season and environment, using a ward D method.

FIGURE 2

Stacked bar plot of the average per cent abundance of taxa and a forest plot legend of the log fold change in taxon abundance for taxa which significantly differed between the faecal microbiome of eastern grey squirrels sampled from an urban and exurban site in both ANCOM‐BC and ALDEx2 tests. Bars represent standard error in taxon difference estimates from ANCOM‐BC tests. Samples from all seasons pooled by environment type.

FIGURE 3

Stacked bar plot of the average per cent abundance of taxa and a forest plot legend of the log fold change in taxon abundance for taxa in the eastern grey squirrel faecal microbiome which significantly differed between seasons in both ANCOM‐BC and ALDEx2 tests. Error bars represent standard error in taxon difference estimates from ANCOM‐BC tests. Samples from urban and exurban environments pooled by season.

FIGURE 4

Scatterplots of urban versus exurban ANCOM‐BC estimated log fold change in genus‐level taxon abundances within the eastern grey squirrel faecal microbiome between (a) autumn and summer, (b) summer and winter, (c) autumn and spring, (d) autumn and winter, (e) spring and summer, and (f) spring and winter. Dotted lines denote 1:1 lines. Solid lines denote lines of best fit with 95% confidence interval shading.