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 became 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 co-occur 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 co-occurring (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 co-occurring P. bonniea
host and symbiont pairings are the result of priority effects.