Dietary input of microbes and host genetic variation shape among-population differences in stickleback gut microbiota

Abstract

To explain differences in gut microbial communities we must determine how processes regulating microbial community assembly (colonization, persistence) differ among hosts and affect microbiota composition. We surveyed the gut microbiota of threespine stickleback (Gasterosteus aculeatus) from 10 geographically clustered populations and sequenced environmental samples to track potential colonizing microbes and quantify the effects of host environment and genotype. Gut microbiota composition and diversity varied among populations. These among-population differences were associated with multiple covarying ecological variables: habitat type (lake, stream, estuary), lake geomorphology and food- (but not water-) associated microbiota. Fish genotype also covaried with gut microbiota composition; more genetically divergent populations exhibited more divergent gut microbiota. Our results suggest that population level differences in stickleback gut microbiota may depend more on internal sorting processes (host genotype) than on colonization processes (transient environmental effects).

Figure 1

Map of Vancouver Island, British Columbia, Canada (lower left box), showing the location of two estuary sample sites, and the Amor de Cosmos watershed. The detailed inset map (upper right) shows the six lake and two stream sites sampled from within the Amor de Cosmos watershed.

Figure 2

(a) By habitat type, the first two axes from a Linear Discriminant Analysis (LDA) describing variation in the first 21 unweighted axes (the number of axes that individually describe at least 1% of variation) from the fish-only PCoA. (b) By population, the first two axes from an LDA describing variation in the first 27 unweighted axes from the lake fish only PCoA.

Figure 3

(a) Number of OTUs shared among stickleback from different habitats after rarefaction to 3000 sequences per individual. (b) Number of OTUs shared among stickleback, invertebrates and water microbiotas after rarefaction to 3000.

Figure 4

Linear regression of genetic divergence (Rst, based on microsatellite allele frequencies reported in Caldera and Bolnick 2008) among six lake populations versus mean microbial phylogenetic distance (mean unweighted UniFrac). Mantel R=0.651, P=0.020.

Figure 5

Alpha diversity levels (# OTUs) of stickleback gut microbiotas after rarefaction to 3000. Metrics phylogenetic diversity, chao1 and species richness all varied among populations: each P<0.001, and F=4.667, 4.452, 5.497, respectively. White=estuary, light gray=stream, dark gray=lake.

Figure 6

Regression of mean lake depth² with mean between-fish unweighted UniFrac distance among the six lake populations, plus upper and lower confidence intervals.