Evolution of mammals and their gut microbes

Abstract

Mammals are metagenomic in that they are composed of not only their own gene complements but also those of all of their associated microbes. To understand the coevolution of the mammals and their indigenous microbial communities, we conducted a network-based analysis of bacterial 16S ribosomal RNA gene sequences from the fecal microbiota of humans and 59 other mammalian species living in two zoos and in the wild. The results indicate that host diet and phylogeny both influence bacterial diversity, which increases from carnivory to omnivory to herbivory; that bacterial communities codiversified with their hosts; and that the gut microbiota of humans living a modern life-style is typical of omnivorous primates.

Figure 1. Network-based analyses of fecal bacterial communities in 60 mammalian species

(A) Simplified cartoon illustration of a host-gut microbe network. Network diagrams are color-coded by (B) diet, (C) animal taxonomy, (D) animal provenance, or represent randomized assignments of OTUs to animal nodes (E). Abbreviations used for animal species (* indicates wild): Asian Elephants, ElephAs1–3; Baboons, Baboon, BaboonW; African Elephants, ElephAf1–4; Bwindi Gorilla, GorillaW; Hartmann’s Mountain Zebra, ZebraW; Armadillo, Arma; Argali Sheep, SheepA1–3; Babirusa, Barb; Seba’s Short tailed Bat, Bat; American Black Bears, BrBear1,2; Bush Dogs, BshDog1,3; Banteng, Banteng; Bighorn Sheep, SheepBH1–3; Black Lemur, BlLemur; Bonobo, Bonobo; Calimicos (Goeldi’s Marmoset), Calimico; Capybara, Capybara; Cheetahs, Cheet2,3; Chimpanzees, Chimp1,12; Eastern Black and White Colobus, BWColob; East Angolan Colobus, BWColobSD; Cattle, Cow1–3; Douc Langur, DcLangur; Echidna, Echidna; Flying Fox, FlyFox; François Langur, FrLangur; Giraffe, Giraffe; Western Lowland Gorillas, Gorilla, GorillaSD; Giant Panda, GtPanda; Geoffrey’s Marmoset, Marmoset; Grevy’s Zebra, GZebra; Humans, HumAdB, HumAdO, HumAdS, HumEckA, HumEckB, HumEckC, HumNag6, HumOldA, HumOldB, HumOldC, HumSuau, HumVeg; HumLC1A, HumLC1B, HumLC2A, HumLC2B; Hedgehog, HgHog; Horses, HorseJ, HorseM; Rock Hyraxes, Hyrax, HyraxSD; Spotted Hyenas, Hyena1,2; Indian Rhinoceros, InRhino; Red Kangaroos, KRoo1,2; Lions, Lion1–3; Mongoose Lemur, MgLemur; Naked Mole rat, Mole rat; Okapi, Okapi1–3; Orangutans, Orang1,2; Polar Bears, PBear1,2; Rabbit, Rabbit; Norway Rat (Wistar), Rat; Black Rhinoceros, BlRhino; Red Pandas, RdPanda, RdPandaSD; Red River Hog, RRHog; Ring Tailed Lemur, RtLemur; White-Faced Saki, Saki; Springboks, SpBok and SpBokSD; Spectacled Bear, SpecBear; Speke’s Gazelles, SpkGaz2,3; Prevost’s Squirrel, Squirrel; Spider Monkey, SpiMonk; Takin, Takin; Transcaspian Urial Sheep, SheepTU1,2; Visayun Warty Pig, VWPig; Somali Wild Ass, WildAss. See Table S1 for additional details.

Figure 2. Mammalian fecal bacterial communities clustered using principal coordinates analysis (PCoA) of the UniFrac metric matrix

PC1 and PC2 are plotted on x- and y-axes. Each circle corresponds to a fecal sample colored according to (A) diet, (B), diet fiber index, (C), gut morphology/physiology and (D) host taxonomic order. The percentage of the variation explained by the plotted principal coordinates is indicated on the axes.

Figure 3. Markers of trophic level mapped onto the variance in fecal microbial community diversity

(A) Stable isotope values for C and N plotted for each fecal sample, presented according to diet group. Symbols are colored according to their PC1 value: PC1 is the first principal coordinate of the PCoA of the unweighted UniFrac metric. δ¹³C ranges for C3 and C4 plants are highlighted in blue. R² is for δ¹³C versus δ¹⁵N. (B) Box plots are shown for the three diet groups (central line is the mean; box outline equals 1 S.D.; the bar denotes 2 S.D.; circles are outliers). The majority of fecal δ¹³C values are intermediate between the average for C4 plants (−12.5%) and C3 plants (−26.7%).