Fidelity in co-diversified symbiosis

Obligate co-dependence can arise in symbiosis, yielding heritable partnerships. These interactions are considered to be highly specific, but partner fidelity is difficult to quantify owing to the experimental constraints of symbiont exchange between host species. Here, we overcome this challenge by leveraging the unique transmission dynamics of Stammera capleta, the obligate digestive symbiont of tortoise beetles (Chrysomelidae: Cassidinae). Despite its extracellular localization, S. capleta possesses a drastically reduced genome ([~]0.25 Mb) and is vertically transmitted through egg-associated spheres. Manipulating these spheres allowed us to experimentally exchange S. capleta between beetle species to determine their impact on host development. We show that non-native S. capleta can successfully colonize the symbiotic organs of a novel host, but that the interaction outcome correlates with genetic relatedness to the native symbiont. Genetically distant species trigger a more pronounced transcriptional response and can only partially rescue host development. While more closely related symbionts proliferate similarly to the native one and induce a comparable host response, they fail to propagate to the next generation, underscoring how transmission fidelity, host-symbiont compatibility, and local adaptation can further specificity within a Paleocene-aged partnership.