Population Genetic Divergence and Environment Influence the Gut Microbiome in Oregon Threespine Stickleback

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.

Keywords: ecology; genetic divergence; host-bacterial associations; microbiome; microbiota; population genomics.

Figure 1

Site map in Oregon. Filled and open points represent freshwater and estuary, respectively. Two inland freshwater populations and four coastal populations were sampled.

Figure 2

Threespine stickleback population genetic structure partitioned between inland and coastal sites, and between estuary and freshwater sites on the coast. This biplot includes the first two principal component (PC) axes, which accounted for more than half (56.19%) of the overall variation in 391 randomly selected genome-wide SNPs for the six populations in this study [37]. Each point represents a fish. Shape fill represents whether sites were in the Willamette Basin (“Inland”) or in watershed along the coast (“Coastal”). Colors represent collection sites (“populations”) in Oregon. Populations in Oregon based on restriction site-associated DNA sequencing (RAD-seq) single nucleotide polymorphisms (SNPs).

Figure 3

Gut microbiome alpha diversity among threespine stickleback populations in Oregon in terms of inverse Simpson diversity (a) and Shannon diversity (b) measures. Colors represent collection sites (“populations”). Each point is a fish gut. Mid-box lines are pooled means of major environments (e.g., Coastal Freshwater”). Box whiskers are pooled standard deviation of major environments, as well.

Figure 4

Gut microbiome beta diversity among threespine stickleback populations in terms of distance-to-centroid transformed: (a) Unweighted UniFrac distance (b) Weighted UniFrac distance. Colors represent collection sites (“populations”). Each point is a fish gut. Mid-box lines are pooled means of major environments (e.g., Coastal Freshwater”). Box whiskers are pooled standard deviation of major environments, as well.

Figure 5

Significant differential ASV abundance in fish gut microbiome was determined between: (a) Inland and coastal regions; (b) and freshwater and estuary environments in Oregon. Each point (darker points are overlapped points) is an ASV that is enriched in a phylum. Negative and positive log₂fold values are enrichments in on either side of x-axis, for example, in estuary and freshwater fish guts, respectively.