Stability and phylogenetic correlation in gut microbiota: lessons from ants and apes

Abstract

Correlation between gut microbiota and host phylogeny could reflect codiversification over shared evolutionary history or a selective environment that is more similar in related hosts. These alternatives imply substantial differences in the relationship between host and symbiont, but can they be distinguished based on patterns in the community data themselves? We explored patterns of phylogenetic correlation in the distribution of gut bacteria among species of turtle ants (genus Cephalotes), which host a dense gut microbial community. We used 16S rRNA pyrosequencing from 25 Cephalotes species to show that their gut community is remarkably stable, from the colony to the genus level. Despite this overall similarity, the existing differences among species' microbiota significantly correlated with host phylogeny. We introduced a novel analytical technique to test whether these phylogenetic correlations are derived from recent bacterial evolution, as would be expected in the case of codiversification, or from broader shifts more likely to reflect environmental filters imposed by factors such as diet or habitat. We also tested this technique on a published data set of ape microbiota, confirming earlier results while revealing previously undescribed patterns of phylogenetic correlation. Our results indicated a high degree of partner fidelity in the Cephalotes microbiota, suggesting that vertical transmission of the entire community could play an important role in the evolution and maintenance of the association. As additional comparative microbiota data become available, the techniques presented here can be used to explore trends in the evolution of host-associated microbial communities.

Cephaloticoccus gen. nov., a new genus of ‘Verrucomicrobia’ containing two novel species isolated from Cephalotes ant guts

“…These symbionts are protected by a proventricular filter (Lanan et al, 2016), remain stable in laboratory-reared colonies and likely coevolved with their hosts (Sanders et al, 2014). 'Verrucomicrobia' belonging to the order Opitutales are consistently detected at high numbers in the ant midgut (Anderson et al, 2012;Hu et al, 2014;Lanan et al, 2016).…”

Temporal variation selects for diet–microbe co-metabolic traits in the gut of Gorilla spp

“…Nonetheless, evidence also suggests that specific microbiome arrangements may arise from environmental triggers, such as diet and geography (Amato et al, 2014a;Gomez et al, 2015). Thus, a reasonable approach to reconstruct the gut microbiomes of primates should consider both evolutionary (host phylogeny) and environmental perspectives (Sanders et al, 2014).…”

Divergence across diet, time and populations rules out parallel evolution in the gut microbiomes of Trinidadian guppies

“…The phylogenetic tree, which was used for unweighted and weighted UniFrac analyses, was constructed in QIIME 1.8 using RAxML (Stamatakis et al, 2005). Because 97% OTU clusters can mask important within and between sample diversity (Eren et al, 2013;Sanders et al, 2014), we further examined genotype/strain variation within 97% OTUs among sampling sites and treatments (see Supplementary Text for analysis).…”