Host traits and environmental variation shape gut microbiota diversity in wild threespine stickleback

Abstract

Background: Despite the growing recognition of the importance of gut microbiota in host ecology and evolution, our understanding of the relative contributions of host-associated and environmental factors shaping gut microbiota composition within and across wild populations remains limited. Here, we investigate how host morphology, sex, genetic divergence, and environmental characteristics influence the gut microbiota of threespine stickleback fish populations from 20 lakes on Vancouver Island, Canada.

Results: Our findings reveal substantial variation in gut microbiota composition and diversity among populations, with host traits exerting a relatively stronger influence on bacterial alpha diversity than environmental characteristics. Previous studies have suggested a link between stickleback body shape and niche specialization, and our results indicate that aspects of host morphology may be associated with gut microbiota divergence among populations, though whether this is related to trophic ecology remains to be explored. Within and across populations, we only observed a weakly defined core microbiota and limited sharing of amplicon sequence variants (ASVs) among hosts, indicating that gut microbiota composition is individualized. Additionally, we detected sex-dependent differences in microbial diversity, opening avenues for future research into the mechanisms driving this variation.

Conclusions: In sum, our study emphasizes the need to consider both host-associated and environmental factors in shaping gut microbiota dynamics and highlights the complex interplay between host organisms, their associated microbial communities, and the environment in natural settings. Ultimately, these insights add to our understanding of the eco-evolutionary implications of host-microbiota interactions while underscoring the need for further investigation into the underlying mechanisms.

Keywords: Gasterosteus aculeatus; 16S rRNA sequencing; Animal microbiome; Gut microbiome.

Fig. 1

Map of Vancouver Island, Canada, showing locations of the 20 lakes included in this study. For each lake the sample size for the corresponding stickleback population is indicated. The lakes are distributed across several watersheds and this map provides an overview of the geographic distribution of the sampled populations. These data allow investigating how ecological, geographic, and environmental factors influence the stickleback gut microbiota

Fig. 2

Taxonomic bar plots on the phylum level summarized by population (A). Alpha diversity, shown as ASV richness, by population (B) and by host sex (C)

Fig. 3

Core gut microbiota (A) and within-population beta diversity across stickleback populations (B). The number of core ASVs at the 50% threshold ranged from 4 to 16 across lakes, while at the 80% threshold, it ranged from 0 to 3 (A). On average, ASVs were shared among 5% to 8.5% of individuals within a population (A). Within-population beta diversity was consistently high across lakes based on unweighted UniFrac, with average values ranging from 0.73 to 0.76 (B). Together, these results demonstrate limited evidence for a core microbiota and high within-population variability across wild stickleback populations on the ASV level (see Table S6 for core bacterial families)

Fig. 4

Principal Coordinates Analysis (PCoA) plot based on the unweighted UniFrac metric illustrating the variation in microbial community composition among fish guts (triangles) and water samples (circles) collected from different lakes. Each point represents a sample with colors indicating the lake of origin. The axes correspond to the first two principal coordinates, which capture the majority of the variance in the data. Ellipses denote the 99% confidence intervals for the clustering of sample types (fish guts and lake water)

Fig. 5

We used multiple regression on distance matrices (MRM) to find whether gut microbiota divergence (beta diversity) on the population is associated with divergence in free-living bacterial communities of the lakes, host morphology and genetics, as well as geographic distance. Each data point represents a pairwise comparison between two populations for gut microbiota beta diversity and stickleback morphology and between two lakes for lake water beta diversity. Population-level beta diversity (based on Bray–Curtis dissimilarity) was explained by host morphological divergence (A) and by divergence in free-living bacterial communities (based on weighted UniFrac) (B). No significant predictors were found for unweighted UniFrac