Sympatric chimpanzees and gorillas harbor convergent gut microbial communities

Abstract

The gut microbial communities within great apes have been shown to reflect the phylogenetic history of their hosts, indicating codiversification between great apes and their gut microbiota over evolutionary timescales. But because the great apes examined to date represent geographically isolated populations whose diets derive from different sources, it is unclear whether this pattern of codiversification has resulted from a long history of coadaptation between microbes and hosts (heritable factors) or from the ecological and geographic separation among host species (environmental factors). To evaluate the relative influences of heritable and environmental factors on the evolution of the great ape gut microbiota, we assayed the gut communities of sympatric and allopatric populations of chimpanzees, bonobos, and gorillas residing throughout equatorial Africa. Comparisons of these populations revealed that the gut communities of different host species can always be distinguished from one another but that the gut communities of sympatric chimpanzees and gorillas have converged in terms of community composition, sharing on average 53% more bacterial phylotypes than the gut communities of allopatric hosts. Host environment, independent of host genetics and evolutionary history, shaped the distribution of bacterial phylotypes across the Bacteroidetes, Firmicutes, Proteobacteria, and Actinobacteria, the four most common phyla of gut bacteria. Moreover, the specific patterns of phylotype sharing among hosts suggest that chimpanzees living in sympatry with gorillas have acquired bacteria from gorillas. These results indicate that geographic isolation between host species has promoted the evolutionary differentiation of great ape gut bacterial communities.[Supplemental material is available for this article.]The compositions of the gut microbial communities harbored by great apes reflect the phylogeny of their hosts in a manner suggesting that host species and their gut microbiota have codiversified over evolutionary timescales Degnan et al. 2012). This pattern of codiversification between hosts and their gut microbiota could stem from both heritable factors, such as host genetics and the vertical, generation-to-generation transmission of gut microbes (Vaishampayan et al. 2010), and environmental factors, such as host diet and geography (Ley et al. 2008a,b;Turnbaugh et al. 2008Turnbaugh et al. , 2009De Filippo et al. 2010;La Serre et al. 2010;Muegge et al. 2011;Claesson et al. 2012;Yatsunenko et al. 2012). However, because the great ape species sampled to date represent populations that are at once phylogenetically, ecologically, and geographically distinct, it has not been possible to separate the relative influences of heritable and environmental factors on the evolution of the great ape gut microbiota.One approach to parsing the effects of environmental factors on the gut microbiota from those of heritable factors is to compare sympatric (i.e., co-occurring) and allopatric (i.e., geographically separated) host populatio...

Bacterial community composition and fermentation in the rumen of Xinjiang brown cattle (Bos taurus), Tarim red deer (Cervus elaphus yarkandensis), and Karakul sheep (Ovis aries)

“…This result was consistent with the findings for other ruminant species, including Bovinae, Cervidae, Caprinae, Camelidae and Giraffidae (Henderson et al 2015). Moreover, the predominant bacteria in the rumen of red deer were similar to those in elk, white-tailed deer, roe deer, sika deer, reindeer and moose (Gruninger et al 2014;Ishaq and Wright 2014;Li et al 2013;Li et al 2014;Sundset et al 2007). This result suggest an effect on rumen microbiota by host genetics (Moeller et al 2013).…”

“…Additionally, metagenomic analyses in the rumen of Svalbard reindeer and sika deer also suggested that Prevotella spp. plays a potential role in cellulose degradation (Li et al 2013;Pope et al 2012). Indeed, Huws et al (2016) The results also showed that Succiniclasticum spp.…”

“…The host-associated microbiota is significantly affected by heritable factors, such as host genetics (Goodrich et al 2014), environmental factors such as the diet composition (Henderson et al 2015;Smith et al 2015), and the geographic location (Moeller et al 2013). Therefore, the rumen microbiota may differ among Xinjiang brown cattle, Karakul sheep and Tarim red deer.…”

“…Pérez-Barberia et al (2004) revealed the rate of evolution of fiber digestibility to be related to climatically driven environmental changes over the past several million years. Moeller et al (2013) showed that geographic isolation among host species promoted evolutionary differentiation in the gut bacterial community of great apes. Considering the main forages of the three studied hosts, including Phragmites communis and Populus diversifolia (Qiao et al 2006), examining rumen fermentation will improve our understanding the roles of the bacterial community.…”

Temporal variation selects for diet–microbe co-metabolic traits in the gut of Gorilla spp

“…This has been an important area of microbiome research since it was first stated that host phylogeny was the main factor explaining gut microbiome composition in different primate species (Ochman et al, 2010;Yildirim et al, 2010). Since then, further evidence has highlighted a more prominent role of diet and digestive modularity in defining gut microbiome composition in primates (Amato et al, 2014b;Gomez et al, 2015;Muegge et al, 2011;Ley et al, 2008;Moeller et al, 2013). However, for the first time, we present inter-species microbiome differences in two different members of the primate order in the context of seasonal dietary variability and microbe-metabolome interactions.…”