Facultative symbiont virulence determines horizontal transmission rate without host strain specificity

Abstract

AbstractIn facultative symbioses, only a fraction of hosts are associated with a symbiont. Understanding why specific host and symbiont strains are associated can inform us of the evolutionary forces affecting facultative symbioses. Possibilities include ongoing host-symbiont coevolution driven by reciprocal selection, or priority effects that are neutral in respect to the host-symbiont interaction. We hypothesized that ongoing host-symbiont coevolution would lead to higher fitness estimates for naturally co-occurring (native) host and symbiont combinations compared to nonnative combinations. We used theDictyostelium discoideum–Paraburkholderia bonnieasystem to test this hypothesis.P. bonnieafeatures a reduced genome size relative to anotherParaburkholderiasymbiont ofD. discoideum, indicating a significant history of coevolution with its host. Facultative symbionts may experience continued genome reduction if coevolution is ongoing, or their genome size may have reached a stable state if the symbiosis has also stabilized. Our work demonstrates that ongoing coevolution is unlikely forD. discoideumandP. bonniea.The system instead represents a stable facultative symbiosis. Specifically associated host and symbiont strains in this system are the result of priority effects, and presently unassociated hosts are simply uncolonized. We find evidence for a virulence-transmission trade-off without host strain specificity, and identify candidate virulence factors in the genomes ofP. bonnieastrains that may contribute to variation in benevolence.Lay summarySymbiotic 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 combinations can be the result of reciprocal adaptation between host and symbiont partners so that naturally co-occurring combinations 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 co-occurring combinations of host and symbiont strains of the social amoebaDictyostelium discoideumand its symbiontParaburkholderia bonniea. Our work demonstrates thatD. discoideumandP. bonnieaare in a stable facultative relationship. Specifically associated host and symbiont combinations are the result of priority effects, andD. discoideumhosts 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 thatP. bonnieasymbionts can spread among amoeba hosts when they aggregate together during the social stage of their life cycle.