Initially Coexisting Endosymbionts Migrate Into Different Tissues During Ontogeny of Host Cicadas

ABSTRACT Endosymbionts play pivotal roles in driving ecological and evolutionary diversification of many insects, yet the morphogenesis and evolutionary origin of their specialised symbiotic organs (e.g., bacteriomes) remain poorly understood. Here we investigated the bacteriome morphogenesis in Cicadidae using microscopy‐based methods. We revealed that bacteriomes originate either from both the original bacteriocytes that emerged after anatrepsis and the novel bacteriocytes that appeared during katatrepsis, or solely from the latter. Bacteriomes expand via “budding” proliferation to increase the bacteriome unit number, and bacteriome developmental patterns closely correlate with the presence/absence of the yeast‐like fungal symbionts (YLS) and their colonisation dynamics. The obligate endosymbiont Karelsulcia and YLS, coexisting in bacteriomes during early stages of host ontogeny, may compete for ecological niches, potentially resulting in translocation of YLS into fat bodies. This indicates that bacteriomes may have initially functioned as immune organs like fat bodies, but evolved specifically for accommodating bacterial endosymbionts. The translocation of YLS from bacteriomes to fat bodies during the later development of host cicadas indicates that immune‐mediated regulation occurs in such symbiotic organs as host insects mature. This study sheds light on how symbiont‐host interactions shape the symbiotic organogenesis, which provides insights into adaptive evolution of specialised symbiotic organs in plant sap‐feeding insects.