Abstract

Wild great apes harbor clades of gut bacteria that are restricted to each host species. Previous research shows the evolutionary relationships among several host-restricted clades mirror those of great-ape species. However, processes such as geographic separation, host-shift speciation, and host-filtering based on diet or gut physiology can generate host-restricted bacterial clades and mimic patterns of co-diversification across host species. To gain insight into the distribution of host-restricted taxa, we examine captive great apes living under conditions where sharing of bacterial strains is readily possible. Here, we show that increased sampling of wild and captive apes identifies additional host-restricted lineages whose relationships are not concordant with the host phylogeny. Moreover, the gut microbiomes of captive apes converge through the displacement of strains that are restricted to their wild conspecifics by human-restricted strains. We demonstrate that host-restricted and co-diversifying bacterial strains in wild apes lack persistence and fidelity in captive environments.

Highlights

  • Wild great apes harbor clades of gut bacteria that are restricted to each host species

  • The gyrase B (gyrB) amplicon data from wild apes (n = 130), captive apes (n = 72), and industrialized humans (n = 16) generated in this study and from published data[5], along with gyrB sequences extracted from metagenomic data from over 9000 humans worldwide[20] (Supplemental data 2), yield a total of 7596 Amplicon Sequence Variants (ASVs) that typed to the Bacteroidales order

  • Based on analyses of both 16S-ASVs and the more highly variable gyrB-ASVs in wild apes, captive apes, and humans, we show that the gut microbiomes of great ape species in captivity change and converge due to both the loss of strains present in their wild conspecifics and the gain of strains that are restricted to humans

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Summary

Introduction

Wild great apes harbor clades of gut bacteria that are restricted to each host species. Hostswitch events can sometimes mimic patterns of co-divergence when related bacterial strains colonize sister species, but they can generate host-restricted microbial clades that erode patterns of codivergence Due to their similar outcomes, differentiating among these processes that underlie the appearance of host-restricted strains is often difficult, but it is necessary for understanding the forces shaping gut microbiome assembly. Captive individuals are separated from their ancestral populations, fed alternative diets, and exposed to bacteria harbored by caretakers and by other species living in close proximity, any of which could act to disrupt the host-microbe associations of their wild conspecifics Under such restrictive conditions, bacterial strains or species that typically inhabit a host can be lost and unrecoverable[13], being displaced by novel bacteria[14] and/or by related strains occupying a similar functional niche[15]. Maintenance of host-restricted bacterial taxa despite dietary and environmental changes, and where inter-species transmission is possible, is compelling evidence of host specialization and co-evolution

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