A role for gut microbiota in host niche differentiation

Abstract

If gut microbes influence host behavioral ecology in the short term, over evolutionary time, they could drive host niche differentiation. We explored this possibility by comparing the gut microbiota of Madagascar’s folivorous lemurs from Indriidae and Lepilemuridae. Occurring sympatrically in the eastern rainforest, our four, target species have different dietary specializations, including frugo-folivory (sifakas), young-leaf folivory (indri and woolly lemurs), and mature-leaf folivory (sportive lemurs). We collected fecal samples, from 2013 to 2017, and used amplicon sequencing, metagenomic sequencing, and nuclear magnetic resonance spectroscopy, respectively, to integrate analyses of gut microbiome structure and function with analysis of the colonic metabolome. The lemurs harbored species-specific microbiomes, metagenomes, and metabolomes that were tuned to their dietary specializations: Frugo-folivores had greater microbial and metagenomic diversity, and harbored generalist taxa. Mature-leaf folivores had greater individual microbiome variation, and taxa and metabolites putatively involved in cellulolysis. The consortia even differed between related, young-leaf specialists, with indri prioritizing metabolism of fiber and plant secondary compounds, and woolly lemurs prioritizing amino-acid cycling. Specialized gut microbiota and associated gastrointestinal morphologies enable folivores to variably tolerate resource fluctuation and support nutrient extraction from challenging resources (e.g., by metabolizing plant secondary compounds or recalcitrant fibers), perhaps ultimately facilitating host species’ diversity and specialized feeding ecologies.

Gut microbiota of frugo-folivorous sifakas across environments

“…For example, plant polyphenols endogenously converted to glucuronides can re-enter the intestinal tract via the biliary route, where they are metabolized by bacterial β- glucuronidases [ 67 ]. In a Malagasy rainforest, folivorous indri consume more foliage than do sympatric frugo-folivorous sifakas [ 68 ] and have greater microbial metagenomic capacity for galactose, glucuronide, and plant-secondary compound metabolism compared to sympatric sifakas [ 69 ]. Although increased glucuronide degradation via gut microbes could relate to substrates other than plant secondary compounds, such findings across lemur species provide further evidence for the microbial response to, and facilitation of, different dietary repertoires across folivorous hosts.…”

“…Beyond contributing evidence to the perturbational effect of captivity on herbivore and folivore gut microbiota [ 6 , 10 , 18 ], we also show that the directionality and strength of effects relate to host-specific feeding strategies [ 15 ]. Herbivores and folivores have specialized diets and, presumably, specialized consortia [ 69 ]. Such host specificity should be an important consideration when designing husbandry strategies, given that the gut microbes of dietary specialists, compared to those of generalists, may be less resilient to the broad dietary challenges introduced under captive conditions.…”

“…Future efforts to alleviate captivity-induced dysbiosis and restore host-microbial symbiosis may require species-specific approaches to naturalizing provisioned diets. Our results across wild sifaka populations show that gut microbiota of folivores are strongly tuned to local conditions [ 27 ] and are as specialized as are their hosts [ 69 ]. Thus, the extreme sensitivity of folivorous specialists, both to captivity [ 59 , 60 , 71 ] and to anthropogenic change [ 72 ], may owe, in part, to co-specialization between hosts and their gut microbes, neither of which can readily adapt to dietary change.…”

I Like the Way You Eat It: Lemur (Indri indri) Gut Mycobiome and Geophagy

“…1 b, c and d, Supplementary Video S1). In the folivorous diet, the interactions between host and gut microbiome are necessary for the processes involved in cellulase activities due to the absence of these enzymes in all vertebrates [6,7]. Primates' gut harbour a plethora of microbes, including archaea, bacteria and fungi, which play a crucial role in the digestion process, health and behaviour [8][9][10][11].…”

Comparative genomic analysis of sifakas ( Propithecus ) reveals selection for folivory and high heterozygosity despite endangered status

“…Gut microbiota are fundamental to folivore and herbivore nutrition, contributing to plant fiber and secondary compound degradation, essential amino acid, vitamin, and nutrient biosynthesis ( 96 ). Previous work has shown the gut microbiota of sifakas to comprise taxa and metabolic processes tuned to their hosts’ specialized diets ( 14 ) and that respond, in real time, to changing diets ( 97 ). The ecological and metabolic success of folivory in sifakas suggests that these lemurs could be prime candidates in which to investigate the coevolution of the genomes of the host organism and its associated microbiota to better understand the shift to novel, digestively challenging feeding strategies.…”