Host evolutionary history and ecological context modulate the adaptive potential of the microbiome

Can the microbiome serve as a reservoir of adaptive potential for hosts? To address this question, we leveraged ~150 generations of experimental evolution in Drosophila melanogaster in a stressful, high-sugar (HS) diet. We performed a fully reciprocal transplant experiment using the control and evolved HS bacteria. If the microbiome confers benefits to hosts, then transplant recipients should gain fitness benefits compared to controls. Interestingly, we found that benefits do exist, but mismatches between fly evolution and microbiome exerted fitness costs by reducing fecundity, especially in the stressful HS diet. The dominant HS bacteria (Acetobacter pasteurianus) uniquely encoded several genes to enable uric acid degradation, mediating the toxic effects of uric acid accumulation due to the HS diet for flies. Our study demonstrates that host genotype x microbiome x environment interactions have substantial effects on host phenotype, highlighting how host evolution and ecological context together shape the adaptive potential of the microbiome.