Abstract The microbiome contributes to many different host traits, but its role in host adaptation remains enigmatic. The fitness benefits of the microbiome often depend on ecological conditions, but theory suggests that fluctuations in both the microbiome and environment modulate these fitness benefits. Moreover, vertically transmitted bacteria might constrain the ability of both the microbiome and host to respond to changing environments. Drosophila melanogaster provides an excellent system to investigate the impacts of interactions between the microbiome and the environment. To address this question, we created field mesocosms of D. melanogaster undergoing seasonal environmental change with and without the vertically transmitted bacteria, Wolbachia pipientis . Sampling temporal patterns in the microbiome revealed that Wolbachia constrained microbial diversity. Furthermore, Wolbachia and a dominant member of the microbiome, Commensalibacter , were associated with differences in two higher‐order fitness traits, starvation resistance and lifespan. Our work here suggests that the interplay between the abiotic context and microbe–microbe interactions may shape key host phenotypes that underlie adaptation to changing environments. We conclude by exploring the consequences of complex interactions between Wolbachia and the microbiome for our understanding of eco‐evolutionary processes that shape host‐microbiome interactions.

Wolbachia impacts microbiome diversity and fitness‐associated traits for Drosophila melanogaster in a seasonally fluctuating environment