Analysis of intestinal microbiota in hybrid house mice reveals evolutionary divergence in a vertebrate hologenome

Abstract

Recent evidence suggests that natural selection operating on hosts to maintain their microbiome contributes to the emergence of new species, that is, the ‘hologenomic basis of speciation’. Here we analyse the gut microbiota of two house mice subspecies, Mus musculus musculus and M. m. domesticus, across their Central European hybrid zone, in addition to hybrids generated in the lab. Hybrid mice display widespread transgressive phenotypes (that is, exceed or fall short of parental values) in a variety of measures of bacterial community structure, which reveals the importance of stabilizing selection operating on the intestinal microbiome within species. Further genetic and immunological analyses reveal genetic incompatibilities, aberrant immune gene expression and increased intestinal pathology associated with altered community structure among hybrids. These results provide unique insight into the consequences of evolutionary divergence in a vertebrate ‘hologenome’, which may be an unrecognized contributing factor to reproductive isolation in this taxonomic group.

Host genetic determinants of the gut microbiota of wild mice

“…To test whether population differences in the gut microbiota were due to the environment or to host genetics, we identified population differences in the gut microbiota that persisted in a common laboratory environment. Consistent with previous studies of wild mice raised in captivity (Wang et al, , ), we observed a decrease in alpha‐diversity and in the relative abundances of Firmicutes and Proteobacteria, and an increase in the relative abundance of Bacteroidetes, in laboratory‐reared animals compared to wild‐caught animals. Despite the changes in gut microbial composition that occurred when progeny of wild mice were raised in the laboratory, population differences persisted among the laboratory‐reared mice.…”

Phylosymbiosis: Relationships and Functional Effects of Microbial Communities across Host Evolutionary History

“…If they exist, disruption of phylosymbiosis via hybridization or microbiota transplants should lead to reduced fitness or performance. For instance, hybridization experiments demonstrate negative interactions or "hybrid breakdown" between host genetics and the gut microbiota that drives intestinal pathology in house mice [65] and severe larval lethality between N. vitripennis and N . giraulti wasps [2].…”

Gut microbiomes of free‐ranging and captive Namibian cheetahs: Diversity, putative functions and occurrence of potential pathogens

“…In our study, among the intrinsic host factors, sex had no effect on the overall microbial community diversity and composition but did affect the abundance of some genera. The determination of the role of sex on the gut microbiome remains challenging, since some recent studies have reported an effect on microbial community composition (Bolnick, Snowberg, Hirsch et al., ; Markle et al., ), but others have not (Degnan et al., ; Wang et al., ). In our study, the five genera Blautia , Eubacterium , Peptococcus , Sutterella and one unclassified genus from Ruminococcaceae were significantly more abundant in males than in females.…”