Bighorn sheep gut microbiomes associate with genetic and spatial structure across a metapopulation

Anna E Jolles,Marci F Witczak,Rachel S Crowhurst,Claire E Couch,Thomas J Sharpton,Clinton W Epps,Holly K Arnold,Brianna R Beechler

doi:10.1038/s41598-020-63401-0

Anna E Jolles, Marci F Witczak + Show 6 more

Open Access

https://doi.org/10.1038/s41598-020-63401-0

Copy DOI

Abstract

Studies in laboratory animals demonstrate important relationships between environment, host traits, and microbiome composition. However, host-microbiome relationships in natural systems are understudied. Here, we investigate metapopulation-scale microbiome variation in a wild mammalian host, the desert bighorn sheep (Ovis canadensis nelsoni). We sought to identify over-represented microbial clades and understand how landscape variables and host traits influence microbiome composition across the host metapopulation. To address these questions, we performed 16S sequencing on fecal DNA samples from thirty-nine bighorn sheep across seven loosely connected populations in the Mojave Desert and assessed relationships between microbiome composition, environmental variation, geographic distribution, and microsatellite-derived host population structure and heterozygosity. We first used a phylogenetically-informed algorithm to identify bacterial clades conserved across the metapopulation. Members of genus Ruminococcaceae, genus Lachnospiraceae, and family Christensenellaceae R7 group were among the clades over-represented across the metapopulation, consistent with their known roles as rumen symbionts in domestic livestock. Additionally, compositional variation among hosts correlated with individual-level geographic and genetic structure, and with population-level differences in genetic heterozygosity. This study identifies microbiome community variation across a mammalian metapopulation, potentially associated with genetic and geographic population structure. Our results imply that microbiome composition may diverge in accordance with landscape-scale environmental and host population characteristics.

Highlights

Studies in laboratory animals demonstrate important relationships between environment, host traits, and microbiome composition
We identified bacterial lineages conserved across a bighorn sheep metapopulation, despite differences between populations in terms of microbiome composition
Differences in microbiome communities correlated with genetic heterozygosity, suggesting that intrinsic host factors play a role in microbial composition even at a metapopulation scale

Summary

Introduction

Studies in laboratory animals demonstrate important relationships between environment, host traits, and microbiome composition. We sought to identify over-represented microbial clades and understand how landscape variables and host traits influence microbiome composition across the host metapopulation To address these questions, we performed 16S sequencing on fecal DNA samples from thirty-nine bighorn sheep across seven loosely connected populations in the Mojave Desert and assessed relationships between microbiome composition, environmental variation, geographic distribution, and microsatellite-derived host population structure and heterozygosity. Studies in humans and laboratory animals have demonstrated that the composition of host-associated gut microbiomes is largely determined by a complex interaction of environment, nutrition, and genetics[3,4,5,6,7,8], suggesting that the microbiome could mediate relationships between environmental variation and health in natural populations.

Methods

Results

Conclusion