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.