Introduction
The gut microbial communities of humans and wild living primates reflect the evolutionary histories of their hosts (Ochman et al. 2010; Moeller et al. 2014; Amato et al. 2019). Each host species’ gut microbiota contains a distinct set of microbial lineages, some of which have co-diversified with primate species (Moeller et al. 2016). However, gut microbial lineages that are confined to geographically separated wild populations of host species can be transmitted between host species when individuals come into direct contact. Similarly, shared environments can lead to the parallel gain or loss of lineages from the gut microbiota in co-occurring host populations, reducing differentiation of the gut microbiota. For example, studies of captive non-human primates (NHPs) have demonstrated that captivity leads to partial convergence of NHP gut microbiota with human gut microbiota (Clayton et al. 2016). In both apes (Uenishi et al. 2007; McKenzie et al. 2017; Frankel et al. 2019; Campbell et al. 2020; Narat et al. 2020) and monkeys (Nakamura et al. 2011; Clayton et al. 2016; McKenzie et al. 2017; Tsukayama et al. 2018; Frankel et al. 2019; Hale et al. 2019; Lee et al. 2019), the gut microbiotas of captive NHP populations are distinct from those of wild populations. In addition, captive the gut microbiotas of captive NHPs are often more compositionally similar to human gut microbiotas than are the gut microbiotas of wild living conspecific NHP populations (Clayton et al. 2016). The disruption and humanization of the endogenous gut microbiota in captive primates has been implicated in the gastrointestinal diseases often experienced by these populations (McKenna et al. 2008; Amato et al. 2016; Shigeno et al. 2018).
Despite the potential importance of humanization of the gut microbiota for the health of captive NHPs, this process, which can proceed through the gain of microbial lineages found in humans or the loss of gut microbiota constituents private to wild NHPs, has not been systematically evaluated across captive NHP populations. It is currently unclear whether humanization of the primate gut microbiota tends to be underlain by specific sets of microbial lineages or whether all lineages in the primate gut microbiota are equally prone to humanization. Similarly, the degree to which the probability of humanization of specific microbial lineages in captivity varies across primate populations and species is unknown.
One limitation of previous studies that has hindered the identification of specific microbial lineages that respond to captivity in NHP species is the lack of population-level host sampling. Several previous studies have examined the effects of captivity in the gut microbiota in multiple NHP species (Nakamura et al. 2011; McKenzie et al. 2017; Tsukayama et al. 2018; Frankel et al. 2019; Hale et al. 2019; Lee et al. 2019), but these have rarely examined more than ten individuals in captivity per NHP species. Sample size is often an insurmountable constraint given the limited sizes of captive NHP populations. Previous studies have had power to detect broad differences in gut microbiota composition between captive and wild populations (e.g., differences in microbiota alpha and beta diversity), but have typically not had power to test for effects of captivity on each individual microbial lineage in the gut microbiota. Another limitation of previous studies has been the lack of replicate captive NHP populations from the sample species, which are required in order to test the reproducibility and predictability of the effects of captivity on the gut microbiota of NHP species. One exception to these limitations is a previous study of wild and captive red-shanked doucs that sampled >30 captive individuals from two replicate captive populations, observing some evidence of reproducible effects of captivity (Clayton et al. 2016). Repeating such sampling regimes, in which relatively large numbers of individuals are sampled from multiple independent conspecific captive populations, in other NHP species promises to reveal whether NHP species display reproducible, NHP-species specific responses to captivity.
Here, we sequenced the gut microbiota of captive chimpanzees retired from the New Iberia Research Center and combined our data with gut microbiota datasets from humans, wild chimpanzees, and additional captive and wild populations of chimpanzees, gorillas, and red-shanked doucs. Each captive and wild population was represented by >15 individuals, enabling tests for differentially abundant microbial lineages between wild and captive individuals as well as microbial signatures of humanization within individual gut microbial clades. Results showed that gut microbial lineages were remarkably consistent in the degree to which they were humanized in replicate captive primate populations from the same species. However, the fraction of the gut microbiota that was humanized in captivity varied significantly among primate species. These results indicate that the sets of microbial taxa that are humanized in the captive primate gut microbiota are predictable but dependent on host species identity.