Diet specialization selects for an unusual and simplified gut microbiota in two- and three-toed sloths

Abstract

Symbiotic microbial communities are critical to the function and survival of animals. This relationship is obligatory for herbivores that engage gut microorganisms for the conversion of dietary plant materials into nutrients such as short-chain organic acids (SCOAs). The constraint on body size imposed by their arboreal lifestyle is thought to make this symbiosis especially important for sloths. Here, we use next-generation sequencing to identify the bacteria present in the fore and distal guts of wild two- and three-toed sloths, and correlate these communities with both diet and SCOAs. We show that, unlike other mammalian herbivores, sloth gut communities are dominated by the bacterial phyla Proteobacteria and Firmicutes. Specifically, three-toed sloths possess a highly conserved, low-diversity foregut community with a highly abundant Neisseria species associated with foregut lactate. In contrast, two-toed sloths have a more variable and diverse foregut microbiota correlated with a variety of SCOAs. These differences support the hypothesis that feeding behaviour selects for specific gut bacterial communities, as three-toed sloths subsist primarily on Cecropia tree leaves while two-toed sloths have a more generalist diet. The less diverse diet and gut microbiota of three-toed sloths may render them more susceptible to habitat loss and other diet-altering conditions.