Significant effects of host dietary guild and phylogeny in wild lemur gut microbiomes

Abstract

Mammals harbor diverse gut microbiomes (GMs) that perform critical functions for host health and fitness. Identifying factors associated with GM variation can help illuminate the role of microbial symbionts in mediating host ecological interactions and evolutionary processes, including diversification and adaptation. Many mammals demonstrate phylosymbiosis-a pattern in which more closely-related species harbor more similar GMs-while others show overwhelming influences of diet and habitat. Here, we generated 16S rRNA sequence data from fecal samples of 15 species of wild lemurs across southern Madagascar to (1) test a hypothesis of phylosymbiosis, and (2) test trait correlations between dietary guild, habitat, and GM diversity. Our results provide strong evidence of phylosymbiosis, though some closely-related species with substantial ecological niche overlap exhibited greater GM similarity than expected under Brownian motion. Phylogenetic regressions also showed a significant correlation between dietary guild and UniFrac diversity, but not Bray-Curtis or Jaccard. This discrepancy between beta diversity metrics suggests that older microbial clades have stronger associations with diet than younger clades, as UniFrac weights older clades more heavily. We conclude that GM diversity is predominantly shaped by host phylogeny, and that microbes associated with diet were likely acquired before evolutionary radiations within the lemur families examined.

Fig. 1. The phylogenetic and ecological diversity of lemur species sampled in this study.

A Lemur phylogeny adapted from Herrera and Dávalos [25]. Bolded tip labels denote species sampled in our study. Colors within squares represent the habitat of the collection site (see Fig. 1B); icons signify food groups that account for at least 20% of the species’ diet (see Table S1). B Map of sampling sites, colored by values provided in the WorldClim “Precipitation of Warmest Quarter” raster layer [59].

Fig. 2. Host phylogenetic relatedness and taxonomic identity significantly contribute to differences in GM beta diversity across samples.

A Co-dendrogram comparison of branching order between the host phylogeny (left) and species-average Jaccard UPGMA tree. B Jaccard PCoA plot coded by host family (shape) and species (color).

Fig. 3. Lemur GM beta diversity shows significant phylogenetic signal.

Here, we demonstrate strength of phylogenetic signal (y-axis) across species-average principal coordinate scores (x-axis). We compared beta diversity metrics (colors) and phylogenetic signal tests (shapes). The horizontal dashed line marks the maximum possible Pagel’s Lambda score (strong phylogenetic signal), as well as the minimum threshold to conclude significant phylogenetic signal using Blomberg’s K.