Wolbachiainteracts with the microbiome to shape fitness-associated traits during seasonal adaptation inDrosophila melanogaster

Abstract

AbstractThe 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 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 melanogasterprovides an excellent system to investigate the evolutionary effects of interactions between the microbiome and the environment. To address this question, we created field mesocosms ofD. melanogasterundergoing seasonal adaptation with and without the vertically transmitted bacteria,Wolbachia pipientis.Sampling temporal patterns in the microbiome revealed thatWolbachiaconstrained microbial diversity. Furthermore, interactions betweenWolbachiaand the microbiome contributed to fitness-associated traits.Wolbachiaoften exerted negative fitness effects on hosts, and the microbiome modulated these effects. Our work supports recent theoretical advances suggesting that hosts in temporally fluctuating environments benefit from flexible microbial associations with low transmission fidelity—specifically when changes in the microbiome can better enable host phenotypes to match environment change. We conclude by exploring the consequences of complex interactions betweenWolbachiaand the microbiome for our understanding of eco-evolutionary processes and the utility ofWolbachiain combating vector-borne disease.