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

Jamieson C. Gorrell,Martin Wu,Ben Dantzer,Andrew G. McAdam,Murray M. Humphries,Stan Boutin,Tiantian Ren,David W. Coltman

doi:10.1186/s40168-017-0382-3

Abstract

BackgroundOur 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.ResultFor 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.ConclusionTaken 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.

Highlights

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
It has been suggested that seasonal variation in gut microbial composition found in wild wood mice [15], ground squirrels [16], and giant pandas [17] are largely driven by the seasonal shifts in diet composition
Red squirrel gut microbiota profile By 16S rRNA gene sequencing, we analyzed the gut microbial communities of North American red squirrels using 905 fecal samples collected from 363 red squirrels

Summary

Introduction

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. It has been suggested that seasonal variation in gut microbial composition found in wild wood mice [15], ground squirrels [16], and giant pandas [17] are largely driven by the seasonal shifts in diet composition. These studies either lacked detailed dietary information in the wild or were performed on animals in captivity. No study has directly assessed the effect of diet on gut microbiota in wild

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