Symbiont interactions with non-native hosts limit the formation of new symbioses

Natalie Niepoth, Jacintha Ellers, Lee M. Henry

Facultative symbionts are common in eukaryotes and can provide their hosts with significant fitness benefits. Despite the advantage of carrying these microbes, they are typically only found in a fraction of the individuals within a population and are often non-randomly distributed among host populations. It is currently unclear why facultative symbionts are only found in certain host individuals and populations. Here we provide evidence for a mechanism to help explain this phenomenon: that when symbionts interact with non-native host genotypes it can limit the horizontal transfer of symbionts to particular host lineages and populations of related hosts. Using reciprocal transfections of the facultative symbiont Hamiltonella defensa into different pea aphid clones, we demonstrate that particular symbiont strains can cause high host mortality and inhibit offspring production when injected into aphid clones other than their native host lineage. However, once established, the symbiont's ability to protect against parasitoids was not influenced by its origin. We then demonstrate that H. defensa is also more likely to establish a symbiotic relationship with aphid clones from a plant-adapted population (biotype) that typically carry H. defensa in nature, compared to clones from a biotype that does not normally carry this symbiont. These results provide evidence that certain aphid lineages and populations of related hosts are predisposed to establishing a symbiotic relationship with H. defensa. Our results demonstrate that host-symbiont genotype interactions represent a potential barrier to horizontal transmission that can limit the spread of symbionts, and adaptive traits they carry, to certain host lineages.