Convergence of gut microbiomes in myrmecophagous mammals

Abstract

Mammals have diversified into many dietary niches. Specialized myrmecophagous (ant-and termite-eating) placental mammals represent a textbook example of evolutionary convergence driven by extreme diet specialization. Armadillos, anteaters, aardvarks, pangolins and aardwolves thus provide a model system for understanding the potential role of gut microbiota in the convergent adaptation to myrmecophagy. Here, we expand upon previous mammalian gut microbiome studies by using high-throughput barcoded Illumina sequencing of the 16S rRNA gene to characterize the composition of gut microbiota in 15 species representing all placental myrmecophagous lineages and their close relatives from zoo-and field-collected samples. We confirm that both diet and phylogeny drive the evolution of mammalian gut microbiota, with cases of convergence in global composition, but also examples of phylogenetic inertia. Our results reveal specialized placental myrmecophages as a spectacular case of largescale convergence in gut microbiome composition. Indeed, neighbour-net networks and beta-diversity plots based on UniFrac distances show significant clustering of myrmecophagous species (anteaters, aardvarks and aardwolves), even though they belong to phylogenetically distant lineages representing different orders. The aardwolf, which diverged from carnivorous hyenas only in the last 10 million years, experienced a convergent shift in the composition of its gut microbiome to become more similar to other myrmecophages. These results confirm diet adaptation to be a major driving factor of convergence in gut microbiome composition over evolutionary timescales. This study sets the scene for future metagenomic studies aiming at evaluating potential convergence in functional gene content in the microbiomes of specialized mammalian myrmecophages.

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

“…As found previously [10][11][12]14], variation in taxonomic composition among wild Malagasy mammals was correlated with both host evolutionary history and diet, depending on the relatedness of the host species. Moreover, shared terrestriality, but not geographic distance between sampling sites, predicted microbiome similarity among distantly related hosts with divergent diets and digestive physiologies.…”

“…We further compared these Malagasy mammalian gut microbiomes to those of 46 other mammal species among 13 host orders [10,12]. Bush pigs and cattle clustered with other members of Artiodactyla, lemurs with other primates, and fossa microbiomes with other carnivores (Fig.…”

“…Several studies of zoo animals reared on artificial diets have claimed that diet and shared environment have greater impacts on gut microbiome composition than endogenous factors [10][11][12][13][14]. Other studies have focused on closely related mammal species and generally found that host species and their gut microbes exhibit concordant relationships [8,[15][16][17][18], with the gut microbial communities of different host species forming distinct clusters [18][19][20].…”

“…However, captivity alters microbiome composition in mammals [12,[29][30][31], and, when animals are compared across geographic regions, host phylogenetic differences may be confounded by differences in local microbial taxa [15,32]. Thus, many of these prior studies did not have sufficient data for resolving the relative influences of various heritable and environmental factors.…”

Convergence in Multispecies Interactions

“…While foregut fermentation evolved separately in ungulates, rodents, marsupials, primates, and birds [30], the bacterial gut community of the hoatzin (the only avian foregut fermenter) is more similar to the gut community of a cow than it is to that of a chicken [32]. Ant and termite-eating vertebrates similarly show convergence of gut microbial communities; in this case, diet is probably the major influence [33]. Gut microbiomes are strongly influenced by both gut morphology and host diet, and distantly related hosts with similar diets tend to independently acquire organisms from the same bacterial phyla [31].…”