Subspecies divergence, hybridisation and the spatial environment shape phylosymbiosis in the microbiome of house mice

Abstract

Closely related host species share similar symbionts, yet how host genetics and the environment affect symbiont communities at different stages of host genetic divergence remains largely unknown. Similarly, it is unclear whether host-symbiont associations result from or contribute to host divergence.We examined the intestinal community of 619 wild-caught mice from Germany’s European house mouse hybrid zone. Here, hybridisation upon secondary contact reflects divergence and could be traced gradually.Temporal and spatial factors were strong predictors of microbiome composition. Subspecies divergence predicted the composition similarity of the overall microbiome, specifically in the bacteria, parasite and fungal components. The effect of hybridisation was generally weak but significant for the fungal component. We confirmed our results in experiments with wild-derived inbred mice: subspecies’ genetic distances and hybridisation predicted the overall microbiome composition, and hybridisation further predicted fungal similarities among individuals. Fungi seemed more stable to the community perturbation of infection than other components of the microbiome.Differences between subspecies were more substantial across different microbiome components than those associated with hybridisation. Diverged microbiomes are a product of host divergence and are maintained by host genetics upon large environmental effects. These results provide a unique perspective into the ecoevolutionary processes shaping phylosymbiosis.

Aberrant microbiomes are associated with increased antibiotic resistance gene load in hybrid mice

“…We found that neither locality nor year of collection were significant predictors of the microbial composition (Beta diversity), while hybridicity explained a low but significant proportion of the overall microbial compositional variance while adjusting for the spatial effects of locality (Permutational multivariate analysis of variance (PERMANOVA), F = 1.38, df = 1, R 2 = 0.003, P = .047) and geographic distance ( Supplement 2 ). Differences in the microbiome of the subspecies and microbiome disruption in hybrids have been observed previously [ 10 , 11 ]. This finding might reflect the association between bacteria and host genetics [ 12 ].…”

“…House mice, with genetically diverse subspecies and microbiome variations [ 5 , 6 ], are a suitable model to investigate the effects of host genetics and bacterial community composition on ARGs. Hybrids between these subspecies show much more extreme high or low infection loads of eukaryotic parasites [ 7 , 8 ] and viruses [ 9 ] as well as the composition of the microbiome [ 10 ] and fungi [ 11 ] than pure subspecies, and are referred to as “transgressive phenotypes.” We studied the European House Mouse Hybrid zone (HMHZ), a semipermeable barrier between Mus musculus musculus and Mus musculus domesticus , to assess the impact of this barrier and hybridization on ARGs through microbiome selection.…”

Spotted hyena gut cross-talks: Symbionts modulate mucosal immunity

“…Previous studies in wild nonhuman primates have also documented associations between parasites and bacteria, which are shaped by host-related and ecological factors [118][119][120] . The role and significance of fungi within the intestinal community remains to be elucidated given the scarcity of studies focusing on this taxonomic group within wildlife guts, but see 35,118 .…”

“…This effect is often attributed to changes in host physiology, particularly immune development, but also behavioural and dietary changes. Additionally, the host environment (biotic and abiotic factors) shapes the composition of gut microbiomes, as seen by spatial and temporal heterogeneities [33][34][35] , the effect of diet 36,37 and social interactions 38,39 . Importantly, the environment interacts with host physiology and genetics, and these interactions might change over time and are as such context dependent 40 .…”