Molecular evolution in bacterial endosymbionts of fungi.

The prediction that progressive coupling of host and symbiont metabolic and reproductive interests leads to reduced mixing of symbiont lineages has been verified extensively in maternally transmitted bacterial endosymbionts of insects. To test whether this prediction is also applicable to associations of bacteria with fungi, we explored patterns of molecular evolution in two lineages of mutualistic endosymbionts of fungi: the Burkholderia endosymbionts of Rhizopus microsporus (Mucormycotina) and Candidatus Glomeribacter gigasporarum endosymbionts of arbuscular mycorrhizal fungi (Glomeromycota). We compared these two lineages with the closely related Candidatus Tremblaya princeps endosymbionts of mealybugs (Hemiptera, Coccoidea, Pseudococcidae) and to free-living Burkholderia species. To make inferences about the life histories of the endosymbionts, we relied on the empirically validated predictions of the nearly neutral theory of molecular evolution that a reduction of the effective population size increases the rate of fixation of slightly deleterious mutations. Our analyses showed that the slightly deleterious mutation accumulation patterns in the Burkholderia endosymbionts of Rhizopus were nearly indistinguishable from those in their free-living relatives. In contrast, Ca. Glomeribacter showed unique patterns of molecular evolution that differentiated them from both the Burkholderia endosymbionts of Rhizopus and from the Ca. Tremblaya endosymbionts of insects. These findings imply that reduced mixing of symbiont lineages is not a universal feature of symbioses between fungi and endocellular bacteria.