Gut microbiota individuality is contingent on temporal scale and age in wild meerkats

Abstract

Inter-individual differences in gut microbiota composition are hypothesized to generate variation in host fitness-a premise for the evolution of host-gut microbe symbioses. However, recent evidence suggests that gut microbial communities are highly dynamic, challenging the notion that individuals harbour unique gut microbial phenotypes. Leveraging a long-term dataset of wild meerkats, we reconcile these concepts by demonstrating that the relative importance of identity for shaping gut microbiota phenotypes depends on the temporal scale. Across meerkat lifespan, year-to-year variation overshadowed the effects of identity and social group in predicting gut microbiota composition, with identity explaining on average less than 2% of variation. However, identity was the strongest predictor of microbial phenotypes over short sampling intervals (less than two months), predicting on average 20% of variation. The effect of identity was also dependent on meerkat age, with the gut microbiota becoming more individualized and stable as meerkats aged. Nevertheless, while the predictive power of identity was negligible after two months, gut microbiota composition remained weakly individualized compared to that of other meerkats for up to 1 year. These findings illuminate the degree to which individualized gut microbial signatures can be expected, with important implications for the time frames over which gut microbial phenotypes may mediate host physiology, behaviour and fitness in natural populations.

Keywords: gut microbiome; host–microbiota interactions; intraclass correlation coefficient; meerkats; repeatability; temporal dynamics.

Figure 1.

ICC measures and 95% confidence intervals for meerkat identity (repeatability), social group membership and year of sample collection on (a) the abundances of 39 genera that were detected in at least 50% of samples, and (b) community phenotypes, including bacterial load, three measures of alpha diversity (observed ASV richness, Shannon diversity and Faith's phylogenetic diversity), and the first axis of variation extracted from ordinations based on three beta diversity distances (weighted UniFrac, unweighted UniFrac and Bray–Curtis). Colours are scaled by their relative effect size (ICC), and greyed out if they are not significant. PD = Faiths phylogenetic alpha diversity. (Online version in colour.)

Figure 2.

Phylogenetic signal in ICC for individual identity (repeatability), social group membership and year of sample collection across 121 ASVs with over 30% prevalence in the overall sample. ASVs for which ICC is higher than average are coloured in red. The major phyla are indicated. (Online version in colour.)

Figure 3.

Temporal trends in ICC (a,b) and ASV turnover between sampling events (c,d) of meerkat gut microbiomes. (a,b) Median ICC (and standard error) of individual identity (repeatability), social group membership and year of sample collection from models predicting the abundances of 121 ASVs when samples are categorized by (a) time intervals between sampling from the same individual; and (b) different meerkat age categories. (c,d) Temporal predictors of ASV turnover between consecutive sampling events from the same individual, extracted from a GAMM, showing the association between ASV turnover and (c) the number of days between samples; and (d) the age of the meerkat at the point of the first sample. (Online version in colour.)

Figure 4.

Beta dissimilarity of meerkat gut microbial communities as a function of sampling interval for samples collected up to 2 years apart, coloured by comparison type (grey, within individual; blue, between individuals from the same social group; and red, between individuals from different social groups) and based on (a) Bray–Curtis; (b) unweighted UniFrac, and (c) weighted UniFrac distances. The dashed grey line indicates the 1 year mark. Lower beta dissimilarity indicates higher similarity in community composition. (Online version in colour.)