Environmental Gradients as a Dominant Force in the Macroevolution of a Host-Associated Marine Bacterium.

Natural selection is imposed by both abiotic environmental filtering and biotic interactions, yet their relative roles in shaping the deep phylogeny of widespread, generalist host-associated bacteria remain unclear. Here, we integrate large-scale phylogenomics, environmental sequencing, functional genomics, and global metagenomic analysis to demonstrate that tidal zonation overrides host association as the dominant macroevolutionary force structuring the marine bacterial genus Ruegeria. Analysis of 533 genomes and 74 global coastal metagenomes reveals that the intertidal-subtidal boundary structures the deepest phylogenetic splits, driving the repeated evolution of distinct ecotypes through independent zonation transitions across global coastlines. These ecotypes possess divergent genomic toolkits: intertidal strains are enriched for genes coding for stress resistance and anaerobic metabolism, whereas subtidal strains specialize in high-affinity nutrient scavenging. Our findings establish that predictable physicochemical gradients act as filters that generate foundational diversity from which specialized host symbionts subsequently emerge, reframing how environmental gradients shape microbial evolution at the eco-evolutionary interface.