Complex co‐evolutionary relationships between cicadas and their symbionts

Abstract

Summary 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.

A Study on Symbiotic Systems of Cicadas Provides New Insights into Distribution of Microbial Symbionts and Improves Fluorescence In Situ Hybridization Technique

“…The primers for the amplification of mitochondrial gene (i.e., COI, COII, Cytb) were the same as previously described (24). Multiple alignments of the nucleotide sequences of both cicada and their obligate symbionts were conducted using the online MAFFT program (https://mafft.cbrc.jp/alignment/server/index.html, accessed on 28 July 2022).…”

“…The molecular phylogenetic analysis uncovered that YLS of cicadas form a clade within the entomoparasitic fungi of the genus Ophiocordyceps, which is regarded as a beneficial symbiont evolved from a pathogenic microorganism [9]. Recently, it was revealed that there were five independent replacement events in the loss of Hodgkinia/acquisition of YLS and seven other separate replacement events of YLS (from an Ophiocordyceps fungus to another Ophiocordyceps fungus) within the sampled taxa of Cicadidae [24]. Genome sequencing of YLS of Meimuna opalifera revealed that the genome of YLS encodes biosynthetic pathways for synthesizing almost all essential amino acids and other nutrients, which is sufficient to compensate for the nutritional services provided by Hodgkinia [9].…”

“…Recently, a new subfamily Derotettiginae was established for the Cicadidae based on phylogenetic analyses of both cicadas and their symbiont Sulcia [26]. By contrast, the phylogeny of YLS and related Ophiocordyceps is generally unparallel to that of host insects, but the phylogeny of partial YLS lineages is concordant with that of host insects [9,24]. Therefore, the phylogeny of Sulcia and that of YLS, as well as related Ophiocordyceps, may provide additional molecular evidence to clarify the coevolutionary history of Cicadidae and the symbionts.…”

Cellular and potential molecular mechanisms underlying transovarial transmission of the obligate symbiont Sulcia in cicadas

“…Some cicada species bear the coresident bacterial symbiont Candidatus Hodgkinia cicadicola (hereafter Hodgkinia) in bacteriocytes of the bacteriomes, which can provide the remaining two EAAs for the host cicadas (McCutcheon et al, 2009a(McCutcheon et al, , 2009bMcCutcheon & Moran, 2010). However, Hodgkinia in some cicada lineages has been replaced by yeast-like fungal symbionts (YLS) harboured in bacteriocytes of the fat bodies (Matsuura et al, 2018;Wang et al, 2022;Wang, Huang, et al, 2021), which is presumed to be able to synthesize almost all the EAAs, vitamins and other metabolites for the host cicadas (Matsuura et al, 2018). During the vertical transmission process, the bacteriome-associated symbionts, especially Sulcia, exhibit extreme shape changes when exocytosed from the bacteriomes to the haemolymph and finally migrate into the terminal oocytes of ovaries (Campbell et al, 2018;Huang et al, 2020;Matsuura et al, 2018;Wang, Huang, et al, 2021).…”

No Transcriptional Compensation for Extreme Gene Dosage Imbalance in Fragmented Bacterial Endosymbionts of Cicadas

“…Following at least 250 million years of strict host-association, Sulcia genomes from distantly related hosts show almost perfect gene co-linearity and very similar gene sets ( Moran et al 2005b ; Bennett and Moran 2015 ) [although a broader sampling of Auchenorrhynchan insects shows that several genomic inversions have occurred in different Sulcia lineages ( Deng et al 2022 )]. Likewise, while several cicada groups have replaced Hodgkinia with fungal endosymbionts, Sulcia is retained in every cicada species examined to date ( Matsuura et al 2018 ; Wang et al 2022b ).…”