Complex co-evolutionary relationships between cicadas and their symbionts

Previous evidence suggests that cicadas lacking Hodgkinia may harbour the yeast-like fungal symbionts (YLS). Here, we reinforce an earlier conclusion that the pathogenic ancestor of YLS independently infected different cicada lineages instead of the common ancestor of Cicadidae. Five independent replacement events in the loss of Hodgkinia/acquisition of YLS and seven other replacement events of YLS (from an Ophiocordyceps fungus to another Ophiocordyceps fungus) are hypothesised to have occurred within the sampled cicada taxa. The divergence time of YLS lineages was later than that of corresponding cicada lineages. The rapid shift of diversification rates of YLS and related cicada-parasitizing Ophiocordyceps began at approximately 32.94 Ma, and the diversification rate reached the highest value at approximately 24.82 Ma, which corresponds to the cooling climate changes at the Eocene-Oligocene boundary and the Oligocene-Miocene transition respectively. Combined with related acquisition/replacement events of YLS occurred during the cooling-climate periods, we hypothesise that the cooling-climate changes impacted the interactions between cicadas and related Ophiocordyceps, which coupled with the unusual life cycle and the differentiation of cicadas may finally led to the diversification of YLS in Cicadidae. Our results contribute to a better understanding of the evolutionary transition of YLS from entomopathogenic fungi in insects.