Abstract

Much of animal-associated microbiome research has been conducted in species for which little is known of their natural ecology and evolution. Microbiome studies that combine population genetic, environment, and geographic data for wild organisms can be very informative, especially in situations where host genetic variation and the environment both influence microbiome variation. The few studies that have related population genetic and microbiome variation in wild populations have been constrained by observation-based kinship data or incomplete genomic information. Here we integrate population genomic and microbiome analyses in wild threespine stickleback fish distributed throughout western Oregon, USA. We found that gut microbiome diversity and composition partitioned more among than within wild host populations and was better explained by host population genetic divergence than by environment and geography. We also identified gut microbial taxa that were most differentially abundant across environments and across genetically divergent populations. Our findings highlight the benefits of studies that investigate host-associated microbiomes in wild organisms.

Highlights

  • Microbiome research is a major area of research in ecology and evolution [1], which is partly due to an increased understanding of the importance of the microbiome to animal fitness [2].Recent microbiome research has frequently focused on the vertebrate gut, for several reasons.The densely colonized and metabolically diverse gut microbiome can influence host nutrition [3]and development [4], including the onset of host immunity [5]

  • We found that microbiome composition was better predicted by fish population genetic divergence than by geographic distance and environment

  • Using principal component analyses (PCA), we found genetic variation in the populations that we sampled was mainly partitioned

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Summary

Introduction

Microbiome research is a major area of research in ecology and evolution [1], which is partly due to an increased understanding of the importance of the microbiome to animal fitness [2].Recent microbiome research has frequently focused on the vertebrate gut, for several reasons.The densely colonized and metabolically diverse gut microbiome can influence host nutrition [3]and development [4], including the onset of host immunity [5]. A normal gut microbiome is important in preventing pathogen infection and many host disorders, such as inflammatory bowel disease and colorectal cancer in humans [6,7,8]. Despite this previous research, we still do not fully understand how host genetics and environmental factors interact to influence the structure and function of an individual animal’s microbiome [9,10]. During the earliest stages of development, most vertebrate hosts are essentially sterile, but enter a world dominated by microbes [11], where they are rapidly colonized [12]

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