The roles of dispersal limitation and pre-adaptation in shaping Paraburkholderia endosymbiont frequencies in social amoeba communities

Abstract

Endosymbiotic interactions have long played fundamental roles in shaping the evolution and diversification of eukaryotes. However, we still have a limited understanding of how ecological processes govern the distribution of endosymbionts that are still segregating in host populations. To contribute to this understanding, here we use the interactions between Paraburkholderia endosymbionts and their Dictyostelid social amoeba hosts as a model system to investigate the role of dispersal, a fundamental ecological process, in shaping the distribution and evolution of endosymbiotic interactions. We first found that patterns of endosymbiont diversification were highly biogeographic, suggesting a significant degree of dispersal limitation. We then experimentally mediated the dispersal of several endosymbiont species into environments with multiple host species and found that each symbiont was able to sustain a high prevalence in each host population. The benefit/detriment of these mediated interactions did not change with increasing phylogenetic distance from what is suspected to be the focal amoeba host species in nature. Taken together, our findings suggest Paraburkholderia endosymbionts are generally pre-adapted to occupy a variety of Dictyostelid host environments, and their distribution among host populations is subject to a high degree of dispersal limitation. Overall, our findings have significant implications for our understanding of how ecological processes facilitate and limit the evolution of endosymbiotic interactions. ImportanceEndosymbiotic interactions are ubiquitous in complex eukaryotes, as organelles such as mitochondria and chloroplasts represent the remnants of what were once free-living prokaryotes. However, how ecological processes facilitate the transition from free-living to host-associated is less understood. Selection is the most commonly invoked process to explain this transition: symbionts that are better at infecting hosts and potentially confer some benefit rise in frequency because they are selected for (and otherwise selected against). However, this only describes one fundamental process that can shape the ecology of symbiotic interactions. Here we present evidence that the importance of dispersal (and its limitations) likely exceeds that of selection in shaping the distribution and frequency of Paraburkholderia endosymbionts in their Dictyostelid social amoeba host communities. These findings highlight the need to consider the interaction between ecological processes, rather than individual processes, when understanding the ecology and evolution of endosymbiotic interactions.