The ecosystem on a leash model in mammalian gut microbiota
The hypothetical framework presented by the ecosystem on a leash model
(Foster et al., 2017) suggests that more host control in distantly
related microbes, illustrated by the Faith’s PD index and Unifrac
distances, should be found in individuals with high MHC diversity. This
pattern was observed, although weakly, in alpha diversity analysis for
the western population, highlighting the importance of the MHC class II
gene above MHC class I and microsatellite markers. It is also worth
noting that this result only involves distantly related microbes,
emphasizing the fact that a phylogenetically diverse microbiota could
lead to the dominance of the fastest growing microbes instead of the
microbes that are most beneficial to the host, lending support to the
ecosystem on a leash model.
Similar more robust trends were found in beta-diversity analysis, where
gut microbial composition was different according to the number of
MHC-II motifs a E-mink possessed and the more distant two E-mink are in
MHC-II haplotype, the more different in rare gut microbiota composition
as well. Mostly negative correlations were observed between microbial
abundance and MHC genes richness and divergence, likewise suggesting
more host control in individuals with high adaptive genetic variation.
This also supports an advantage in balancing selection despite strong
genetic drift. The differential abundance analysis also revealed
stronger host control in the western population, mostly explained by the
presence of specific MHC-II motifs. Moreover, the MHC-II gene was more
likely to impact a wide range of microbial taxa. These results are in
line with previous studies conducted on fish, mice and birds (Bolnick et
al., 2014; Khan et al., 2019; Leclaire et al., 2018). However, we did
observe that one motif of MHC-II present in the eastern population also
impacted the abundance of several bacterial families, indicating that
the captive eastern population still possess interesting motifs for host
control.
Because the MHC-I gene targets intracellular non-self-molecules
recognition, it would impact a smaller number of bacteria compared to
MHC-II (Ost & Round, 2018). Other taxonomic groups such as viruses and
protists would need to be targeted for further investigation, and
eastern population might be more equipped to recognize them, given the
increased diversity for this MHC-I gene (Kubinak et al., 2012). This is
of particular importance knowing the circulation of several viruses in
free-ranging western E-mink (Fournier-Chambrillon et al., 2004; Philippa
et al., 2008; Mañas et al., 2016). In particular the canine distemper
virus, which results in a high mortality rate in E-mink, is currently
re-emerging in many wild carnivore populations in Europe (Origgi et al.,
2012) and has had a major impact on population of E-mink in Navarre,
Spain (Fournier-Chambrillon et al., 2021).
Overall, our prediction that less host control will be observed in mink
with lower genetic diversity is supported by both alpha and beta
diversity for the E-mink. However, both populations have low genetic
diversity, and the MHC class II DRB gene seemed to have a stronger
influence in gut microbes than other markers. To further validate our
results, replicating the study to see if those differences are
observable when individuals from the two populations are kept in the
same facility to control for the influence of the external environment
should be conducted. Given that we only had access to samples from a
small fraction of the captive eastern population, our results might also
not be representative of the entire captive breeding stock. Despite the
gut microbiota variation being a complex puzzle, our study gives more
importance to host immunogenetics in the context of species
conservation.