Seasonal, spatial, and maternal effects on gut microbiome in wild red squirrels

Abstract

Background: Our understanding of gut microbiota has been limited primarily to findings from human and laboratory animals, but what shapes the gut microbiota in nature remains largely unknown. To fill this gap, we conducted a comprehensive study of gut microbiota of a well-studied North American red squirrel (Tamiasciurus hudsonicus) population. Red squirrels are territorial, solitary, and live in a highly seasonal environment and therefore represent a very attractive system to study factors that drive the temporal and spatial dynamics of gut microbiota.

Result: For the first time, this study revealed significant spatial patterns of gut microbiota within a host population, suggesting limited dispersal could play a role in shaping and maintaining the structure of gut microbial communities. We also found a remarkable seasonal rhythm in red squirrel's gut microbial composition manifested by a tradeoff between relative abundance of two genera Oscillospira and Corpococcus and clearly associated with seasonal variation in diet availability. Our results show that in nature, environmental factors exert a much stronger influence on gut microbiota than host-associated factors including age and sex. Despite strong environmental effects, we found clear evidence of individuality and maternal effects, but host genetics did not seem to be a significant driver of the gut microbial communities in red squirrels.

Conclusion: Taken together, the results of this study emphasize the importance of external ecological factors rather than host attributes in driving temporal and spatial patterns of gut microbiota in natural environment.

Keywords: Biogeography; Dispersal; Microbial ecology.

Fig. 1

Bacterial composition of 549 red squirrel fecal samples from grid KL (from 2008 to 2010). Each column represents one sample. Y-axis values represent the relative abundance of each bacterial taxon. Samples are sorted by the sampling time. a Phylum level. b Genus level

Fig. 2

a Relative abundance and prevalence of bacterial genera in red squirrel microbiota. The top ten most abundant genera are labeled with their genus names. b Bacterial genera showing strong seasonal rhythms. X-axis indicates the fluctuation amplitudes, and Y-axis indicates the statistical significance of the rhythm. The size of dot represents the average relative abundance of each genus

Fig. 3

Oscillation of two core genera Coprococcus and Oscillospira over time. Samples were from the grid KL and binned by month. The error bar represents +/− one standard error of the mean

Fig. 4

Distance-decay of the red squirrel gut microbial communities within and between grids. Each dot represents a comparison between samples collected at different geographic locations. Y-axis represents the microbiota similarity. The lines denote the linear regressions of microbial similarity over the geographic distance

Fig. 5

Red squirrel gut microbiota exhibit individuality and maternal effects. Box-and-whisker plots show pairwise Jaccard distances within each relationship groups. Significance values are from non-parametric Kruskal-Wallis tests (FDR adjusted). *P < 0.05, **P < 0.01, ***P < 0.001