Facultative symbiont virulence determines horizontal transmission rate without host specificity in Dictyostelium discoideum social amoebas

In facultative symbioses, only a fraction of hosts are associated with symbionts. Specific host and symbiont pairings may be the result of host-symbiont coevolution driven by reciprocal selection or priority effects pertaining to which potential symbiont is associated with a host first. Distinguishing between these possibilities is important for understanding the evolutionary forces that affect facultative symbioses. We used the social amoeba, Dictyostelium discoideum, and its symbiont, Paraburkholderia bonniea, to determine whether ongoing coevolution affects which host-symbiont strain pairs naturally cooccur within a facultative symbiosis. Relative to other Paraburkholderia, including another symbiont of D. discoideum, P. bonniea features a reduced genome size that indicates a significant history of coevolution with its host. We hypothesized that ongoing host-symbiont coevolution would lead to higher fitness for naturally cooccurring (native) host and symbiont pairings compared to novel pairings. We show for the first time that P. bonniea symbionts can horizontally transmit to new amoeba hosts when hosts aggregate together during the social stage of their life cycle. Here we find evidence for a virulence-transmission trade-off without host specificity. Although symbiont strains were significantly variable in virulence and horizontal transmission rate, hosts and symbionts responded similarly to associations in native and novel pairings. We go on to identify candidate virulence factors in the genomes of P. bonniea strains that may contribute to variation in virulence. We conclude that ongoing coevolution is unlikely for D. discoideum and P. bonniea. The system instead appears to represent a stable facultative symbiosis in which naturally cooccurring P. bonniea host and symbiont pairings are the result of priority effects. Dictyostelium discoideum amoebas are predators of soil bacteria, but some amoebas also host symbiotic Paraburkholderia bacteria. We use fitness comparisons of native vs. novel host and symbiont pairings to understand the evolutionary forces affecting facultative symbiotic relationships. We also show that P. bonniea symbionts can spread to new amoeba hosts when hosts aggregate together during the social stage of their life cycle and that less virulent P. bonniea strains are more successful at this horizontal transmission. Symbiotic relationships between hosts and their microbial partners are prolonged and intimate associations. Some of these relationships are obligatory for both a host and symbiont to survive, while others are facultative and each partner can survive without the other. In the latter case, some host individuals may be associated with a symbiont while others are not. Specific host and symbiont pairings can be the result of reciprocal adaptation between host and symbiont partners so that naturally cooccurring pairings are best suited for each other in terms of their biological fitness. On the other hand, the symbiont that a host is associated with may simply be the symbiont that arrived first, in what is called a priority effect. We sought to determine which possibility best explained naturally cooccurring pairings of host and symbiont strains of the social amoeba Dictyostelium discoideum and its symbiont Paraburkholderia bonniea. Our work demonstrates that D. discoideum and P. bonniea are in a stable facultative relationship. Specific host and symbiont pairings appear to be the result of priority effects, and D. discoideum hosts without symbionts are simply uncolonized. This work fills a gap in our understanding of the evolutionary forces affecting facultative symbiotic relationships. We also show for the first time that P. bonniea symbionts can spread to new amoeba hosts when hosts aggregate together during the social stage of their life cycle.