Ecological plasticity in the gastrointestinal microbiomes of Ethiopian Chlorocebus monkeys

Abstract

Human activities can cause habitat degradation that may alter the types and quality of available food resources and thus influence the microbiomes of wild animal populations. Furthermore, seasonal shifts in food availability may cause adaptive responses in the gut microbiome to meet the need for different metabolic capabilities. Here, we demonstrate local-scale population structure in the gastrointestinal microbiotas of Chlorocebus monkeys, in southern Ethiopia, in response to varying degrees of human encroachment. We further provide evidence of adaptation to ecological conditions associated with the dry and wet seasons, and show seasonal effects to be more pronounced in areas with limited human activity. Finally, we report species-level microbiota differences between the endemic Ethiopian Bale monkey, an ecological specialist, and generalist Chlorocebus species from the same geographical region.

Extensive variability in the gut microbiome of a highly‐specialized and critically endangered lemur species across sites

“…In general, we found that microbial OTUs clustered according to location and that prokaryotic α diversity was highest in the most pristine site and significantly lower in sites with a history of disturbance. Within the primate clade, similar patterns have been described in the Chlorocebus genus (Trosvik et al, ), Alouatta pigra (Amato et al, ), Lemur catta (Bennett et al, ), and Procolobus gordonorum (Barelli et al, ). GM robustness to habitat disturbance has been reported in parrots ( Strigops habroptilus ; see Perry, Digby, & Taylor, ), but other taxa, including frogs ( Fejervarya limnocharis ; see Chang, Huang, Lin, Huang, & Liao, ), jackals ( Canis mesomelas ; see Menke et al, ), and swan geese ( Anser cygnoides ; see Wu et al, ) show that populations in disturbed habitats exhibit distinct GMs relative to pristine habitat counterparts.…”

“…Several studies show that diet plays a crucial role in shaping the GM throughout an individual's life (Clayton et al, ; David et al, ; De Filippo et al, ; Trosvik, Rueness, de Muinck, Moges, & Mekonnen, ; Turnbaugh, Bäckhed, Fulton, & Gordon, ) and over evolutionary timescales (Gomez et al, ; Groussin et al, ; Ley et al, ; Springer et al, ; Trosvik et al, ; Yildirim et al, ). Anthropogenic disturbance is expected to impact food availability in tropical habitats through changes to microclimates that drive variation in species composition (Abbas et al, ; Arrigo‐Nelson, ; Herrera, Wright, Lauterbur, Ratovonjanahary, & Taylor, ).…”

Shifting Climates, Foods, and Diseases: The Human Microbiome through Evolution

“…For instance, in black howler monkeys (Alouatta pigra), seasonal shifts in gut microbiome SCFA production appear to allow hosts to maintain energy balances despite reduced dietary energy intake. [33][34][35] In some cases, these differences reflect losses of microbial taxa, particularly SCFA producers, which may reduce the potential for microbial buffering of host nutritional stress. Although many modern human populations exhibit limited dietary seasonality, evidence of seasonal microbiome dynamics has been reported in some instances.…”

“…[31,32] Additionally, many primate species exhibit diet-driven differences in gut microbiome composition across habitats. [33][34][35] In some cases, these differences reflect losses of microbial taxa, particularly SCFA producers, which may reduce the potential for microbial buffering of host nutritional stress. [33] Interestingly, species that exhibit this microbial sensitivity to habitat change also have smaller geographic distributions.…”

“…[87] While currently an understudied topic in mammals, a small amount of data suggest that hybridization of two primate species can result in an "intermediate" microbial phenotype. [35] In cases where the functions provided by these gut microbes were beneficial to host fitness, we would expect retention of these microbial lineages. Therefore, alternating or combinatorial genetic and microbial processes likely influenced each other reciprocally, and ultimately shaped human adaptation to local environments.…”