Horizontal transmission and recombination maintain forever young bacterial symbiont genomes

When bacterial symbionts become associated with their hosts, their genomes are thought to decay inexorably towards an organelle-like fate due to decreased recombination and inefficient selection. Despite extensive theoretical treatment, no empirical study thus far has connected these underlying population genetic processes with long-term evolutionary outcomes. By sampling marine endosymbionts that range from primarily vertical to strictly horizontal transmission, we tested this canonical theory. We found that transmission mode strongly predicts recombination rates, and that exceedingly low recombination rates are associated with genome degradation in the marine symbionts with nearly strict vertical transmission. Nonetheless, even the most degraded marine endosymbiont genomes are occasionally horizontally transmitted and are much larger than their terrestrial insect symbiont counterparts. Therefore, horizontal transmission and recombination enable intermediate symbiont genome sizes that maintain substantial functional genetic variation.