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

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.Electronic supplementary materialThe online version of this article (10.1186/s40168-017-0382-3) contains supplementary material, which is available to authorized users.

System Biology Modeling with Compositional Microbiome Data Reveals Personalized Gut Microbial Dynamics and Keystone Species

“…Additionally, we observed cyclic behavior of biomass trajectories in multiple individuals, similar to the seasonal patterns reported in hunter-gatherers of western Tanzania 57 , and the evolutionarily conserved patterns observed in other mammals 58 . Similar patterns have not been reported before for western city dwellers, perhaps due to the confounding effects of aggregate analysis across individuals and the impact of highly diverse diets.…”

Comparative analysis of microbiota along the length of the gastrointestinal tract of two tree squirrel species (Sciurus aberti and S. niger) living in sympatry

“…Most importantly, our conclusions are based on a relatively small number of female animals captured during a narrow time window. Previous studies in wild squirrel populations have shown that gut microbial communities differ between the sexes and vary seasonally (Ren et al, ). Thus, additional sampling from both sexes, along with dietary analysis, would help to more rigorously evaluate hypotheses that we propose.…”

Species identity dominates over environment in shaping the microbiota of small mammals

“…; Ren et al . ). While genetic effects on the gut microbiota have been detected in laboratory and human studies (Wang et al .…”

“…When mice are cohoused, their microbiota composition converges (Hildebrand et al 2013;Seedorf et al 2014;Griffin et al 2017), and cohabiting, unrelated humans are more similar in their gut microbiota than those living apart (Song et al 2013). Strong environmental effects have also been reported in studies of wild animals, including seasonal and habitat differences (Maurice et al 2015;Amato et al 2016;Ren et al 2017). While genetic effects on the gut microbiota have been detected in laboratory and human studies (Wang et al 2018), these are often rather weak, and within-species studies typically emphasise the strong influence of environmental factors, such as diet (Carmody et al 2015;Rothschild et al 2018;Weissbrod et al 2018).…”