Parallel Evolution of Bacteroidota as Long-Term Endosymbionts of Insects.

Symbiotic relationships significantly transform both symbiont and host biology. The most visible changes include a massive reduction of the endosymbiont genome and the development of specialized host organs, cells, and compartments for symbiont housing. However, insect symbiosis studies have often focused on Pseudomonadota or specific symbiosis stages, limiting our understanding of how symbiont diversity arises from particular microbial clades, how the symbiont genomes evolve, and the consequences of symbiosis for diverse host-symbiont pairs. Scale insects, which have experienced repeated gains and losses of nutritional symbionts, provide an ideal evolutionary playground for tracking parallel transitions of insect symbionts originating from the same bacterial phylum. Using extensive genome sampling across the scale insect phylogeny, we recapitulated the path of Bacteroidota transitioning from recently established host-associated bacteria to highly specialized insect endosymbionts with minimal gene sets. Their genomes exhibit strikingly parallel degradation across all gene categories, with some stochastic differences in essential genes for genetic processing and amino acid biosynthesis. Imaging methods further revealed that the symbiotic cells and organs exhibit a trend from more dispersed bacteriocytes to highly compact bacteriomes, closely localized to the host's digestive system. Our results outline a recurrent path by which insect symbioses independently arise, are maintained for up to several hundred million years, and are replaced by new symbionts. The gradual nature of the process implies that the outcomes of symbiosis initially depend on how "professional" vs. "naïve" the host and symbiont are. Over evolutionary time, compatible host-symbiont lineages emerge from these interactions and become preferred.