Hierarchical mode of evolution in freshwater SAR11 driven by species dispersal and lake history

Abstract Microorganisms dominate aquatic ecosystems, yet the evolutionary forces shaping their biogeography remain poorly understood. Freshwater habitats, acting as “isolated islands", may generate distinct evolutionary patterns in contrast to globally connected marine systems. Here, we investigated the globally abundant freshwater SAR11 genus Fontibacterium using a comparative population genomics framework. We analysed genome-wide single nucleotide variants (SNVs) from three species with contrasting dispersal capacities: an African endemic ( F. africanum ), a temperate specialist ( F. temperatum ), and a cosmopolitan species ( F. commune ). All species exhibited significant lake-specific population structure, but the scale of differentiation was constrained by their dispersal potential, ranging from complete genetic isolation between ancient lakes in the endemic species to transcontinental cohesion in the cosmopolitan one. Notably, the cosmopolitan species showed near-complete genetic cohesion between antipodal populations (Japan and Brazil) suggesting stochastic long-distance dispersal without geographic barriers. Furthermore, population genetic signatures varied among lake systems, especially elevated nucleotide diversity and pN/pS ratios in ancient African lakes suggesting relaxed purifying selection; a pattern that may reflect their unique evolutionary history. These findings support a hierarchical model where a species' dispersal capacity sets the broad-scale potential for gene flow, while local lake history determines the fine-scale genetic structure of its populations.