Diverse domestic settings alter the structure and functional potential of pig gut microbial communities and drive ecological variation in pig immunity

Background/Question/Methods

Plasticity in microbiome composition and metabolic activity can impact host physiology, in turn influencing if and how hosts adapt to environmental change. With novel diets, pathogen exposure, and antibiotics, domestication is known to alter the microbiome through environmental change as well as through artificial selection. To what extent microbial plasticity in response to domestication impacts host health remains unclear. We investigated how domestication impacts the gut microbiome and its impact on one aspect of host health – immunity – in genetically wild and domestic pigs living in a variety of environments. To do so, we characterized gut microbial composition and functional potential from 120 pigs in free-ranging wild, free-ranging domestic, captive wild, and captive domestic settings, and measured select immune features, including concentrations of host cytokines and fecal IgA. Given the low fiber diets and increased use of antibiotics in domestication, we hypothesized that pigs in captive settings will have decreased microbial diversity and an increased prevalence of antibiotic resistance genes compared to free-ranging pigs.

Results/Conclusions

Domestication setting explained more variation in microbial community composition compared to species and sampling location (PERMANOVA, F-statistic = 12.1, R2=0.21, p-value < 0.001). Gut microbial functional potential also differed between wild and domestic pigs, with notably higher starch and sucrose metabolism and antibiotic resistance genes found in the gut microbiomes of domestic individuals compared to wild individuals. Domestication setting was also a driver of host immune phenotypes. Across all domestication settings, fecal IgA concentrations were positively correlated with microbial diversity (Spearman correlation, p = 0.56, p-value < 0.001). Indeed, captive domestic pigs demonstrated the highest fecal IgA concentrations, while captive wild pigs had the lowest concentrations (ANOVA, F=6.97, p-value < 0.001) and harbored the lowest microbial diversity (Kruskal-Wallis x2 = 8.77, df = 3, p-value < 0.05). Together, these data suggest that changes in pig gut microbial communities are specific to domestication settings and may correspond to ecological variation in pig immunity. Whether the microbial and immune features promoted by domestication are adaptive in the human environment remains to be tested.