The Evolutionary Consequences of Host-Microbe Interactions: Rapid seasonal evolution of multiple host phenotypes mediated by associated microbes
Authors: Jack Beltz; Paul Schmidt
Affiliation: University of Pennsylvania
Keywords: Experimental evolution
Adaptive evolution is a complex process that is shaped by countless biotic and abiotic interactions between a population and its environment. The relative contributions of these forces and their ultimate impact on evolutionary trajectories are only beginning to be understood. Tracking the influence of host-associated microbes on their host population can offer valuable insight into the role interacting organisms can play in dictating the adaptive landscape of a population. To determine the influence of microbial interactions on host trait evolution, we constructed replicate populations from a panel of D. melanogaster lines collected from local Pennsylvania orchards, which evolved in parallel to seasonal change under different microbial treatments in a natural setting. The microbial treatments included Drosophila-derived Acetobacter and Lactobacillus taxa, which are known to colonize the host and influence phenotypes. The bacterial treatments were inoculated directly onto the population's fruit-based (nutritionally low) food supply, in an effort to maintain an environmentally relevant context. Various host phenotypes, as well as host and environmental microbiome composition, were tracked as these populations evolved in 18 replicate outdoor mesocosms for 115 days (June - November). During this period we observed a significant effect of the microbial treatments on the evolutionary trajectory of multiple life-history phenotypes, compared to control populations that did not receive microbial additions. By early fall the microbial treatment populations had evolved greater starvation resistance, egg to adult viability, adult body size, and lipid concentration as well as shorter larval development time. Additionally, we identified consistent variation across season and treatment, in the composition of the host microbiome. These results demonstrate that interactions between the host and both microbial isolates, effectively “rescue” the phenotypic effect of flies reared under the realistic nutrient stress of a fruit-based diet, potentially altering their fitness in a natural context. The variation in microbiome composition observed across seasonal time and microbial treatment suggests an influence of the host's internal and external environment on its microbial composition. Taken together, we demonstrate that shifts in the abundance of critical microbial taxa can have wide-reaching effects on host trait evolution, microbial composition, and adaptive landscape.