Anthropogenic Disturbance Impacts Gut Microbiome Homeostasis in a Malagasy Primate

Abstract

Increasing anthropogenic disturbances in Madagascar are exerting constrains on endemic Malagasy lemurs and their habitats, with possible effects on their health and survival. An important component of health is the gut microbiome, which might be disrupted by various stressors associated with environmental change. We have studied the gut microbiome of gray-brown mouse lemurs (Microcebus griseorufus), one of the smallest Malagasy primates and an important model of the convergent evolution of diseases. We sampled two sites: one situated in a national park and the other consisting of a more disturbed site around human settlement. We found that more intense anthropogenic disturbances indeed disrupted the gut microbiome of this lemur species marked by a reduction in bacterial diversity and a shift in microbial community composition. Interestingly, we noted a decrease in beneficial bacteria (i.e., members of the Bacteroidaceae family) together with a slight increase in disease-associated bacteria (i.e., members of the Veillonellaceae family), and alterations in microbial metabolic functions. Because of the crucial services provided by the microbiome to pathogen resistance and host health, such negative alterations in the gut microbiome of mouse lemurs inhabiting anthropogenically disturbed habitats might render them susceptible to diseases and ultimately affecting their survival in the shrinking biodiversity seen in Madagascar. Gut microbiome analyses might thus serve as an early warning signal for pending threats to lemur populations.

Assessing the gut microbiome and the influence of host genetics on a critically endangered primate, the Northern muriqui (Brachyteles hypoxanthus)

“…Anthropogenic disturbances are known to heavily impact wildlife populations in a plethora of forms, including changes in host microbiomes (Zhu et al, 2021). Disruptions in the gut microbiome composition have been demonstrated, including the domestication and 'humanization' of the wildlife gut microbiome (Dillard et al, 2022;Prabhu et al, 2020), and the shift in the microbiota community composition due to an increase in disease-associated taxa and a decrease of bene cial bacteria (Wasimuddin et al, 2022). On top of that, population bottlenecks lead to the loss of genetic variation, increased inbreeding and therefore, resulting in a less diverse microbiome.…”

Gut microbiota of white-headed black langurs (Trachypithecus leucocephalus) in responses to habitat fragmentation

“…There are significant differences in gut microbiota of rhesus macaques ( Macaca mulatta ) distributed in different geographical populations being grouped by altitude conditions, which is manifested by the production of new and unique microbiota ( Zhao et al, 2018 ). Additionally, a decreased diversity in the gut microbiota of primates has been observed in gray–brown mouse lemurs ( Microcebus griseorufus ), which may be associated with varying degrees of human invasion of each habitat, occurring in Bale monkeys ( Chlorocebus djamdjamesis ) as well ( Trosvik et al, 2018 ; Wasimuddin et al, 2022 ). The abundance of beneficial gut microbiota and functional metabolism genes is linked to the health of the species, with those in worse habitats showing a decreasing trend, which indicates that these individuals have a more potential disease risk ( Amato et al, 2013 ; Barelli et al, 2015 ; Trosvik et al, 2018 ; Wasimuddin et al, 2022 ).…”

“…Additionally, a decreased diversity in the gut microbiota of primates has been observed in gray–brown mouse lemurs ( Microcebus griseorufus ), which may be associated with varying degrees of human invasion of each habitat, occurring in Bale monkeys ( Chlorocebus djamdjamesis ) as well ( Trosvik et al, 2018 ; Wasimuddin et al, 2022 ). The abundance of beneficial gut microbiota and functional metabolism genes is linked to the health of the species, with those in worse habitats showing a decreasing trend, which indicates that these individuals have a more potential disease risk ( Amato et al, 2013 ; Barelli et al, 2015 ; Trosvik et al, 2018 ; Wasimuddin et al, 2022 ). Furthermore, the differences in the gut microbiota of animals living in different habitats are an outcome of adaptive alterations in response to ecological changes and behavioral adjustments, notably dietary composition ( Wu et al, 2011 ; McManus et al, 2021 ).…”

Effects of forest urbanization on the interplay between small mammal communities and their gut microbiota

“…However, many of these studies have focused on a single host species (e.g. Fackelmann et al, 2021; Stothart et al, 2019; Sugden et al, 2020; Teyssier et al, 2018; Phillips et al, 2018; Wasimuddin et al, 2022). The few studies that investigated GM variations within host communities led to incongruent patterns with either a stronger impact of host phylogeny over habitats on GM assembly (e.g.…”