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.