Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes

Abstract

Over the past decade several studies have reported that the gut microbiomes of mammals with similar dietary niches exhibit similar compositional and functional traits. However, these studies rely heavily on samples from captive individuals and often confound host phylogeny, gut morphology, and diet. To more explicitly test the influence of host dietary niche on the mammalian gut microbiome we use 16S rRNA gene amplicon sequencing and shotgun metagenomics to compare the gut microbiota of 18 species of wild non-human primates classified as either folivores or closely related non-folivores, evenly distributed throughout the primate order and representing a range of gut morphological specializations. While folivory results in some convergent microbial traits, collectively we show that the influence of host phylogeny on both gut microbial composition and function is much stronger than that of host dietary niche. This pattern does not result from differences in host geographic location or actual dietary intake at the time of sampling, but instead appears to result from of differences in host physiology. These findings indicate that mammalian gut microbiome plasticity in response to dietary shifts over both the lifespan of an individual host and the evolutionary history of a given host species is constrained by host physiological evolution. Therefore, the gut microbiome cannot be considered separately from host physiology when describing host nutritional strategies and the emergence of host dietary niches.

Terrestriality and bacterial transfer: a comparative study of gut microbiomes in sympatric Malagasy mammals

“…Bushpig and cattle microbiomes were enriched with Tenericutes, Planctomycetes, and Lentisphaerae whereas fossa microbiomes were deficient in Bacteroidetes and showed higher abundances of microbial taxa related to Firmicutes and Fusobacteria (SAMseq analysis, FDR-adjusted P < 0.0001; Table S2). Consistent with a recent microbiome study on folivorous primates [60], the microbiomes of sifaka and sportive lemurs included significantly higher proportions of unclassified reads at the phyla level (P < 0.0001; Table S2; sifaka: x = 0.03 ± 0.01 s.d. reads per sample; sportive lemurs: x = 0.33 ± 0.01), perhaps due to their remarkably different diet from that of humans.…”

Characterizing symbiont inheritance during host–microbiota evolution: Application to the great apes gut microbiota

“…In the great apes gut microbiota, we found that the major part of the microbiota (91.6%) is constituted of bacteria which acquisition scenario is not distinguishable from one that is independent from the great apes phylogeny (Amato et al, ; Moeller et al, ). Still, we identified OTUs representing 8.4% of the total number of reads that are transmitted across generations during millions of years of evolution.…”

“…HOME is currently best suited to the study of microbiota transmission in recent, well‐sampled host clades in which no or few extinctions occurred, since it does not account for unsampled host lineages, nor for host extinctions. For example, HOME would be well adapted to the study of microbiota transmission in some vertebrates and invertebrate clades, for which microbiota sequencing data are already available (Amato et al, ; Brooks, Kohl, Brucker, van Opstal, & Bordenstein, ; Ren, Kahrl, Wu, & Cox, ). Ignoring extinction is reasonable at the small evolutionary scales of such groups or the great apes (Ochman et al, ), but it would not be at larger evolutionary timescales such as across invertebrate or vertebrate species; in this case, accounting for host switches from now‐extinct lineages is necessary (Szöllosi et al, ).…”

Species identity dominates over environment in shaping the microbiota of small mammals

“…; Amato et al . ; Nishida & Ochman ). Furthermore, recent work has provided evidence for cospeciation among mammals and their gut microbes (Moeller et al .…”