Gut microbiota of frugo-folivorous sifakas across environments

Abstract

Background Captive animals, compared to their wild counterparts, generally harbor imbalanced gut microbiota owing, in part, to their altered diets. This imbalance is particularly striking for folivores that fundamentally rely on gut microbiota for digestion, yet rarely receive sufficient dietary fiber in captivity. We examine the critically endangered Coquerel’s sifaka (Propithecus coquereli), an anatomically specialized, rather than facultative, folivore that consumes a seasonal frugo-folivorous diet in the wild, but is provisioned predominantly with seasonal foliage and orchard vegetables in captivity. Using amplicon and metagenomic sequencing applied to fecal samples collected from two wild and one captive population (each comprising multiple groups), we clarify how dietary variation underlies the perturbational effect of captivity on the structure and function of this species’ gut microbiota. Results The gut microbiota of wild sifakas varied by study population, most notably in community evenness and in the abundance of diet-associated microbes from Prevotellaeceae and Lachnospiraceae. Nevertheless, the differences among wild subjects were minor compared to those evident between wild and captive sifakas: Unusually, the consortia of captive sifakas were the most diverse, but lacked representation of endemic Bacteroidetes and metagenomic capacity for essential amino-acid biosynthesis. Instead, they were enriched for complex fiber metabolizers from the Firmicutes phylum, for archaeal methanogens, and for several metabolic pathways putatively linked to plant fiber and secondary compound metabolism. Conclusions The relatively minor differences in gut microbial structure and function between wild sifaka populations likely reflect regional and/or temporal environmental variability, whereas the major differences observed in captive conspecifics, including the loss of endemic microbes, but gain in low-abundance taxa, likely reflect imbalanced or unstable consortia. Indeed, community perturbation may not necessarily entail decreased community diversity. Moreover, signatures of greater fiber degradation indicate that captive sifakas consume a more fibrous diet compared to their wild counterparts. These results do not mirror those typically reported for folivores and herbivores, suggesting that the direction and strength of captivity-induced ‘dysbiosis’ may not be universal across species with similar feeding strategies. We propose that tailored, species-specific dietary interventions in captivity, aimed at better approximating naturally foraged diets, could functionally ‘rewild’ gut microbiota and facilitate successful management of diverse species.

The gut microbiome of exudivorous marmosets in the wild and captivity

“…Translocated hosts seem to importantly represent a dynamic transitional state between the relative extremes of wild and captive environments, which induce changes in host gut microbiome diversity. Overall, previous studies agree that dietary differences between host captive and wild environments are one of the main factors driving some of these gut microbiome changes 5 , 13 – 18 , 18 , 19 , 69 , 70 .…”

“…More closely related hosts seem to share more similar microbiome communities than more distantly related hosts (i.e., phylosymbiosis) 6 , 7 , and gut microbiome communities are usually enriched for bacteria associated with the main macronutrients of a host’s feeding strategy 8 – 12 . Yet, environmental factors significantly alter individual host microbiomes 10 , 12 , as evidenced by differences in microbiome composition between wild and captive conspecifics across a variety of animal taxa 13 – 19 . Gut microbiome studies of captive and wild mammals show that non-human primates (NHPs) experience relatively large losses of native gut microbiome diversity in captivity compared to the wild 5 , 13 .…”

The Gut Microbiome of Exudivorous Marmosets in the Wild and Captivity

“…More closely related hosts seem to share more similar microbiome communities than more distantly related hosts (i.e., phylosymbiosis) 6,7 , and gut microbiome communities are usually enriched for bacteria associated with the main macronutrients of a host's feeding strategy [8][9][10][11][12] . Yet, environmental factors significantly alter individual host microbiomes 10,12 , as evidenced by differences in microbiome composition between wild and captive conspecifics across a variety of animal taxa [13][14][15][16][17][18][19] . Gut microbiome studies of captive and wild mammals show that non-human primates (NHPs) experience relatively large losses of native gut microbiome diversity in captivity compared to the wild 5,13 .…”

The Gut Microbiome of 54 Mammalian Species

“…High-throughput sequencing technology has made it possible to gain insight into the gut microbiota of a diverse range of animal species, including primates (Amato et al, 2013 ; Clayton et al, 2016 ; Greene et al, 2021 ), carnivores (An et al, 2017 ), reptiles (Tang et al, 2020 ), and birds (Roggenbuck et al, 2014 ; García-Amado et al, 2018 ), among others. The majority of all microbiome studies have been conducted on single species, which provide excellent conditions for investigating short-term exposure effects such as diet changes.…”

“…A number of studies have compared the microbiota of wild and captive animals. Studies in diverse animal species, including Antarctic seals (Nelson et al, 2013 ), various primates (Amato et al, 2013 ; Hale et al, 2019 ; Greene et al, 2021 ), and horses ( Equus ferus caballus ) (Metcalf et al, 2017 ) showed significant differences in the composition of the gut microbiota in wild individuals compared to captive relatives. Another study showed that primates living in captivity gain a more human-like microbiota composition over time (Clayton et al, 2016 ), and that this is reproducible between captive populations (Houtz et al, 2021 ).…”