Fungal and bacterial endosymbionts of eared leafhoppers of the subfamily Ledrinae (Hemiptera: Cicadellidae)

In general, leafhoppers (Hemiptera: Cicadellidae) possess a pair of bacteriomes in the abdomen, which harbor two types of obligate bacterial symbionts: a very ancient Sulcia symbiont and another ancient Nasuia-allied co-symbiont (or a younger Baumannia co-symbiont). However, when we inspected three eared leafhoppers of the subfamily Ledrinae, namely Ledra auditura Walker, Ledropsis discolor (Uhler) and Tituria angulata (Matsumura), L. discolor harbored only Sulcia symbiont while L. auditura and T. angulata possessed no bacterial symbionts. Instead, all the species possessed specialized cells full of yeast-like fungal symbionts within fat bodies. Molecular phylogenetic analysis revealed that the fungal symbionts are placed within the entomoparasitic fungal genus Ophiocordyceps (Ascomycota: Hypocreales: Ophiocordycipitaceae). These results suggest the possibility that (1) the fungal symbiont was acquired in the evolutionary course of the Ledrinae, (2) the original fungus was likely an entomoparasite of the genus Ophiocordyceps, (3) the fungal symbiont replaced the Nasuia-allied symbiont in an ancestral lineage, and (4) even the ancient Sulcia symbiont was finally lost and taken over by the fungal symbiont. Meanwhile, the possibility of multiple independent fungal acquisitions from closely related entomoparasitic Ophiocordyceps fungi cannot be excluded. Our finding uncovers an evolutionary process from a prokaryotic essential symbiosis to a eukaryotic one.