Gut microbes and host dietary niche differentiation
Gut microbes are metabolically versatile and help their hosts digest challenging food. But, can gut microbes also help their hosts avoid feeding competition by facilitating adaptation to specialized diets? We asked in four species of folivorous lemur living sympatrically in a Malagasy rainforest.
Madagascar is a biodiversity hotspot and the only home to some 110 species of lemur. Just under half of all lemur species practice some type of folivory: These leaf eaters stem from six genera and three families, including the woolly lemurs (Avahi spp.), sifakas (Propithecus spp.), and indri (Indri indri) from Indriidae, the bamboo lemurs (Hapalemur spp. and Prolemur simus) from Lemuridae, and the sportive lemurs (Lepilemur spp.) from Lepilemuridae.
Across Madagascar’s forests, species from these lineages variably live in sympatry and avoid competition, in part, by specializing on different folivorous resources: Sifakas practice frugo-folivory; indri and woolly lemurs are, respectively, flexible and dedicated young-leaf folivores; bamboo lemurs specialize on bamboo; and somehow, sportive lemurs survive predominantly on mature leaves.
For folivorous lemurs, the gut microbiome is a critical part of dietary success. Gut microbes break down plant fibers and defensive compounds, and synthesize vitamins and nutrients. To allow space and time for microbial actions, Madagascar’s folivores boast complex gastrointestinal systems, that reflect each species’ dietary specialization.
Figure 1: Features and gut microbiota of four folivorous lemur species that live sympatrically in Madagascar's eastern rainforests. Shown in (a) are color-coded photographs and geographic ranges of diademed sifakas (yellow), indri (light green), eastern woolly lemurs (dark green), and weasel sportive lemurs (teal), with the red dot pinpointing the study site; illustrations of the species’ diets, with the relative size of fruits, flowers, young and mature leaves corresponding to their relative dietary proportion; and features of the species’ gastrointestinal morphology. Shown in (b) are pie charts of the species’ gut microbiota, color-coded by microbial phylum and genus. Photographs kindly provided by Nick Garbutt (nickgarbutt.com); illustrations kindly provided by Sally Bornbusch.
Although microbial contributions to folivore nutrition are broadly established, we know less about how gut microbes might help hosts become specialists on particular folivorous resources, which in turn, might enable dietary niche differentiation in sympatric species.
We studied four folivorous lemur species in the same Malagasy rainforest, including the indri, and one species each of sifaka, woolly lemur, and sportive lemur. We collected 89 fecal samples from 67 lemurs and analyzed them via amplicon and metagenomic sequencing and nuclear magnetic resonance spectroscopy. When integrated together, these analytical approaches yield information about gut microbial structure and function.
We found that the lemurs harbored strikingly species-specific gut microbiomes, metagenomes, and metabolomes that were tuned to each species’ dietary specialization and gastrointestinal morphology.
Frugo-folivorous sifakas had diverse consortia that were similarly structured across individuals, and were enriched for generalist bacteria, metabolic pathways, and metabolites that reflected their consumption of fruits and leaves. In contrast, the mature-leaf specialist sportive lemurs had simple consortia that were variable across individuals. They harbored taxa and metabolites putatively linked to cellulolysis.
The young-leaf specialists had consortia that appeared intermediate between these extremes, but were nevertheless distinct. Indri showed an unusual reliance on Proteobacteria and the microbial metabolism of plant defensive compounds. Woolly lemurs harbored taxa associated with fat and protein, and seemingly prioritized amino acid cycling.
Our results demonstrate that related folivorous species, characterized by different gastrointestinal morphologies, yet living sympatrically, each depend on the metabolic capacity of a unique set of microbes, some of which are highly specialized. We suggest that these species’ distinct gut microbiota and gastrointestinal systems help them differentially withstand plant fibers or defensive compounds, balance fruit and foliage fermentation, and cope with resource fluctuation.
We further suggest that folivory encompasses a greater diversity of feeding strategies than is generally recognized and that gut microbes can facilitate resource partitioning in sympatric species. Ultimately, these findings illuminate how microbes may promote the evolution of feeding specialization and the maintenance of macro-species diversity.For more information, please check out our article: https://www.nature.com/articles/s41396-020-0640-4
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