Abstract
Many animals benefit from microbial symbionts that aid digestion, supply essential nutrients, or provide defense. When this dependence becomes obligate, as in gutless marine oligochaetes that have lost both digestive and excretory systems and rely entirely on their bacterial partners for nutrition and recycling of waste compounds, it would seem to constrain ecological and evolutionary flexibility. Yet, these worms are globally distributed and thrive across diverse environments. To investigate how stability and adaptability coexist in such obligate symbioses, we combined global sampling with high-resolution phylogenomic analyses of 246 individuals from 63 species across 17 marine sites. Ancestral reconstructions revealed that the chemoautotrophic primary symbiont “
Candidatus
Thiosymbion” was acquired early and persistently maintained, whereas additional partners were repeatedly gained through convergent evolution, expanding metabolic potential. Symbiont communities were highly consistent within host species, but this stability dissolved rapidly as hosts diverged, with communities reshaping rapidly across short macroevolutionary timescales. Even the primary symbiont “
Ca
. Thiosymbion” showed low fidelity and occasional displacement, a sharp contrast to other multipartite symbioses, where core partners persist unchanged for hundreds of millions of years. Thus, gutless oligochaetes illustrate how long-term stability at microevolutionary scales can coexist with rapid reshaping at macroevolutionary scales in multipartite symbioses. More broadly, this pattern demonstrates how the paradox of stability through flexibility may underpin the persistence and diversification of complex symbioses across deep time.