Abstract
The vertebrate gut microbiota is a critical determinant of organismal function, yet whether and how gut microbial communities affect host fitness under natural conditions remains largely unclear. We characterised associations between a fitness proxy—individual growth rate—and bacterial gut microbiota diversity and composition in threespine stickleback fish introduced to large semi‐natural ponds. We detected a 63% higher richness of bacterial taxa (α‐diversity) in the guts of high‐fitness fish compared to low‐fitness fish, which might be driven by stronger bacterial dispersal among high‐fitness fish according to the fit of a neutral community model. Further, microbial communities of high‐fitness fish were more similar to one another (i.e., exhibited lower β‐diversity) than those of low‐fitness fish. The lower β‐diversity found to be associated with higher host fitness is consistent with the Anna Karenina principle—that there are fewer ways to have a functional microbiota than a dysfunctional microbiota. Our study links differences in α‐ and β‐diversity to a fitness‐related trait in a vertebrate species reared under naturalistic conditions and our findings provide a basis for functional tests of the fitness consequences of host‐microbiota interactions.