Symbiont evolutionary history underpins quality to an insect host.

While many insects have evolved mechanisms to ensure the faithful transmission of bacterial symbionts across generations, the majority of insects lack such mechanisms. Instead, many insects must acquire symbionts from their local environments. Without mechanisms for vertical transmission, insects are thought to be at risk of experiencing low fitness by acquiring low-quality symbiont strains. For example, insects dependent on environmental symbiont transmission may acquire nonsymbiotic bacteria or symbionts that are adapted to other co-localized hosts. Yet, insects often appear capable of interacting with a wide variety of symbiont strains, and environmental transmission is prevalent across diverse insect species. Therefore, it remains unclear whether the evolutionary history of a symbiont actually impacts its benefit to hosts. Here, we test whether the recent evolutionary history of a symbiont impacts its quality to an insect host by inoculating Anasa tristis De Geer (Hemiptera: Coreidae) insects with Burkholderiaceae strains isolated from a conspecific host, a distantly related heterospecific host, and from soil. We find that the soil strain offers few fitness benefits. In contrast, both strains with a recent history of host association support insect survival to adulthood, but the greatest benefits emerge from the symbiont isolated from a conspecific host, which also improves insect development rates. Overall, our study demonstrates that the evolutionary history of a symbiont may impact its quality to insect hosts and lays a foundation for future work to further examine whether environmental transmission carries costs for insect hosts.