Rarity and reproductive biology drive population genomics of obligate symbioses

Modern perspectives on obligate symbioses increasingly recognize their dynamism, complexity, and global importance. Population genomics has been key to this advancement, yet the extension of existing frameworks to reproducibly integrate across multiple genotype-phenotype-environment relationships remains elusive. We generated 962 metagenomes for six lichens, obligate symbioses between fungi and algae, with contrasting traits sampled at a landscape scale. Core neutral population metrics were primarily driven by rarity and reproductive biology, while genes underlying expression regulation were under selection in response to land use and climate across all species. Examined within a comparative framework, these results illustrate that symbiont interactions are a major factor influencing microevolutionary trajectories, especially neutral processes. We present a conceptual framework for population-scale evolution in obligate symbioses that centers on biotic interactions.