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We present a high-quality assembly and annotation of the periodical cicada species, Magicicada septendecula (Hemiptera: Auchenorrhyncha: Cicadidae). Periodical cicadas have a significant ecological impact, serving as a food source for many mammals, reptiles, and birds. Magicicada are well known for their massive emergences of 1 to 3 species that appear in different locations in the eastern United States nearly every year. These year classes (“broods”) emerge dependably every 13 or 17 yr in a given location. Recently, it has become clear that 4-yr early or late emergences of a sizeable portion of a population are an important part of the history of brood formation; however, the biological mechanisms by which they track the passage of time remain a mystery. Using PacBio HiFi reads in conjunction with Hi-C proximity ligation data, we have assembled and annotated the first whole genome for a periodical cicada, an important resource for future phylogenetic and comparative genomic analysis. This also represents the first quality genome assembly and annotation for the Hemipteran superfamily Cicadoidea. With a scaffold N50 of 518.9 Mb and a complete BUSCO score of 96.7%, we are confident that this assembly will serve as a vital resource toward uncovering the genomic basis of periodical cicadas’ long, synchronized life cycles and will provide a robust framework for further investigations into these insects.

 

Host-microbe interactions are intimately linked to eukaryotic evolution, particularly in sap-sucking insects that often rely on obligate microbial symbionts for nutrient provisioning. Cicadas (Cicadidae: Auchenorrhyncha) specialize on xylem fluid and derive many essential amino acids and vitamins from intracellular bacteria or fungi (Hodgkinia,Sulcia, andOphiocordyceps) that are propagated via transmission from mothers to offspring. Despite the beneficial role of these non-gut symbionts in nutrient provisioning, the role of beneficial microbiota within the gut remains unclear. Here, we investigate the relative abundance and impact of host phylogeny and ecology on gut microbial diversity in cicadas using 16S ribosomal RNA gene amplicon sequencing data from 197 wild-collected cicadas and new mitochondrial genomes across 38 New Zealand cicada species, including natural hybrids between one pair of two species. We find low abundance and a lack of phylogenetic structure and hybrid effects but a significant role of elevation in explaining variation in gut microbiota.

 

Periodical cicadas (Hemiptera:Magicicada) have coevolved with obligate bacteriome-inhabiting microbial symbionts, yet little is known about gut microbial symbiont composition or differences in composition among allochronicMagicicadabroods (year classes) which emerge parapatrically or allopatrically in the eastern United States. Here, 16S rRNA amplicon sequencing was performed to determine gut bacterial community profiles of three periodical broods, including II (Connecticut and Virginia, 2013), VI (North Carolina, 2017), and X (Maryland, 2021, and an early emerging nymph collected in Ohio, 2017). Results showed similarities among all nymphal gut microbiomes and between morphologically distinct 17-yearMagicicada, namelyMagicicada septendecim(Broods II and VI) and 17-yearMagicicada cassini(Brood X) providing evidence of a core microbiome, distinct from the microbiome of burrow soil inhabited by the nymphs. Generally, phylaBacteroidetes[Bacteroidota] (> 50% relative abundance),Actinobacteria[Actinomycetota], orProteobacteria[Pseudomonadota] represented the core.Acidobacteriaand generaCupriavidus,Mesorhizobium, andDelftiawere prevalent in nymphs but less frequent in adults. The primary obligate endosymbiont,Sulcia(Bacteroidetes), was dominant amongst core genera detected.Chryseobacteriumwere common in Broods VI and X.Chitinophaga, Arthrobacter, andRenibacteriumwere common in Brood X, andPedobacterwere common to nymphs of Broods II and VI. Further taxonomic assignment of unclassifiedAlphaproteobacteriasequencing reads allowed for detection of multiple copies of theHodgkinia16S rRNA gene, distinguishable as separate operational taxonomic units present simultaneously. As major emergences of the broods examined here occur at 17-year intervals, this study will provide a valuable comparative baseline in this era of a changing climate.

 

Apart from model organisms, 13- and 17-year periodical cicadas (Hemiptera: Cicadidae: Magicicada) are among the most studied insects in evolution and ecology. They are attractive subjects because they predictably emerge in large numbers; have a complex biogeography shaped by both spatial and temporal isolation; and include three largely sympatric, parallel species groups that are, in a sense, evolutionary replicates. Magicicada are also relatively easy to capture and manipulate, and their spectacular, synchronized mass emergences facilitate outreach and citizen science opportunities. Since the last major review, studies of Magicicada have revealed insights into reproductive character displacement and the nature of species boundaries, provided additional examples of allochronic speciation, found evidence for repeated and parallel (but noncontemporaneous) evolution of 13- and 17-year life cycles, quantified the amount and direction of gene flow through time, revealed phylogeographic patterning resulting from paleoclimate change, examined the timing of juvenile development, and created hypotheses for the evolution of life-cycle control and the future effects of climate changeon Magicicada life cycles. New ecological studies have supported and questioned the role of prime numbers in Magicicada ecology and evolution, found bidirectional shifts in population size over generations, quantified the contribution of Magicicada to nutrient flow in forest ecosystems, and examined behavioral and biochemical interactions between Magicicada and their fungal parasites and bacterial endosymbionts. 

Rapid species radiations present difficulties for phylogenetic reconstruction due to lack of phylogenetic information and processes such as deep coalescence/incomplete lineage sorting and hybridization. Phylogenomic data can overcome some of these difficulties. In this study, we use anchored hybrid enrichment (AHE) nuclear phylogenomic data and mitochondrial genomes recovered from AHE bycatch with several concatenated and coalescent approaches to reconstruct the poorly resolved radiation of the New Zealand cicada species in the generaKikihiaDugdale andMaoricicadaDugdale. Compared with previous studies using only three to five Sanger‐sequenced genes, we find increased resolution across our phylogenies, but several branches remain unresolved due to topological conflict among genes. Some nodes that are strongly supported by traditional support measures like bootstraps and posterior probabilities still show significant gene and site concordance conflict. In addition, we find strong mito‐nuclear discordance; likely the result of interspecific hybridization events in the evolutionary history ofKikihiaandMaoricicada.

 

Contamination of a genetic sample with DNA from one or more nontarget species is a continuing concern of molecular phylogenetic studies, both Sanger sequencing studies and next-generation sequencing studies. We developed an automated pipeline for identifying and excluding likely cross-contaminated loci based on the detection of bimodal distributions of patristic distances across gene trees. When contamination occurs between samples within a data set, a comparison between a contaminated sample and its contaminant taxon will yield bimodal distributions with one peak close to zero patristic distance. This new method does not rely on a priori knowledge of taxon relatedness nor does it determine the causes(s) of the contamination. Exclusion of putatively contaminated loci from a data set generated for the insect family Cicadidae showed that these sequences were affecting some topological patterns and branch supports, although the effects were sometimes subtle, with some contamination-influenced relationships exhibiting strong bootstrap support. Long tip branches and outlier values for one anchored phylogenomic pipeline statistic (AvgNHomologs) were correlated with the presence of contamination. While the anchored hybrid enrichment markers used here, which target hemipteroid taxa, proved effective in resolving deep and shallow level Cicadidae relationships in aggregate, individual markers contained inadequate phylogenetic signal, in part probably due to short length. The cleaned data set, consisting of 429 loci, from 90 genera representing 44 of 56 current Cicadidae tribes, supported three of the four sampled Cicadidae subfamilies in concatenated-matrix maximum likelihood (ML) and multispecies coalescent-based species tree analyses, with the fourth subfamily weakly supported in the ML trees. No well-supported patterns from previous family-level Sanger sequencing studies of Cicadidae phylogeny were contradicted. One taxon (Aragualna plenalinea) did not fall with its current subfamily in the genetic tree, and this genus and its tribe Aragualnini is reclassified to Tibicininae following morphological re-examination. Only subtle differences were observed in trees after the removal of loci for which divergent base frequencies were detected. Greater success may be achieved by increased taxon sampling and developing a probe set targeting a more recent common ancestor and longer loci. Searches for contamination are an essential step in phylogenomic analyses of all kinds and our pipeline is an effective solution. [Auchenorrhyncha; base-composition bias; Cicadidae; Cicadoidea; Hemiptera; phylogenetic conflict.]

 

Abstract Historically, most North American periodical cicada (Hemiptera: Cicadidae: Magicicada spp. Davis 1925) distribution records have been mapped at county-level resolution. In recent decades, Magicicada brood distributions and especially edges have been mapped at a higher resolution, aided by the use of GIS technology after 2000. Brood VI of the 17-yr cicadas emerged in 2000 and 2017 and is the first for which detailed mapping has been completed in consecutive generations. Overlaying the records from the two generations suggests that in some places, Brood VI expanded its range slightly between 2000 and 2017, although the measured changes are close to the lower limit of detectability given the methods used. Even so, no simple alternative to range expansion easily accounts for these observations. We also bolster Alexander and Moore’s assertion that M. cassini does not occur in Brood VI. 

Abstract If all nucleotide sites evolved at the same rate within molecules and throughout the history of lineages, if all nucleotides were in equal proportion, if any nucleotide or amino acid evolved to any other with equal probability, if all taxa could be sampled, if diversification happened at well-spaced intervals, and if all gene segments had the same history, then tree building would be easy. But of course, none of those conditions are true. Hence, the need for evaluating the information content and accuracy of phylogenetic trees. The symposium for which this historical essay and presentation were developed focused on the importance of phylogenetic support, specifically branch support for individual clades. Here, I present a timeline and review significant events in the history of systematics that set the stage for the development of the sophisticated measures of branch support and examinations of the information content of data highlighted in this symposium. [Bayes factors; bootstrap; branch support; concordance factors; internode certainty; posterior probabilities; spectral analysis; transfer bootstrap expectation.] 

A recent paper by Ruschel & Campos (2019) on “leaf-winged” cicadas proposed a significant reorganization of the cicada tribe Hemidictyini Distant, 1905g, including synonymization of the monogeneric tribe Lacetasini Moulds & Marshall, 2018 following the results of a cladistic parsimony analysis of morphological characters. In this study, we reconsider and revise the morphological analysis of Ruschel & Campos and obtain new genetic data for Hemidictya. We find that their study suffers from a limited taxon sample, inappropriate outgroup selection, and misinterpretation of genitalic characters (uncus vs. claspers). We show that Hemidictyini sensu Ruschel & Campos includes members of multiple tribes and subfamilies, and we conclude that some of the taxonomic transfers by Ruschel & Campos are not supported. The two most similar and leaf-like cicadas, Hemidictya Burmeister, 1835 (South America) and Hovana Distant, 1905g (Madagascar), are probably not closely related but rather an excellent example of convergent evolution. Lacetasini is not a junior synonym of the Hemidictyini but a distinct part of the Tettigomyiinae Distant, 1905g as originally classified. We return or transfer the genera Lacetas Karsch, 1890, Iruana Distant, 1905g, Bafutalna Boulard, 1993, and Murphyalna Boulard, 2012 to the Lacetasini. With the transfer of all genera of Iruanina Boulard, 1993 and Bafutalnina Boulard, 1993 to Lacetasini and with Lacetas transferred to the Iruanina, Lacetasini n. syn. becomes a subjective junior synonym of Iruanini rev. stat. in the Tettigomyiinae. We assign Hovana to Hovanini n. tribe in the Tettigomyiinae and Sapantanga Distant, 1905g to Sapantangini n. tribe in the Tibicininae Distant, 1905b. We propose that Hemidictyini sensu novo contains only the genus Hemidictya and we assign the tribe to Tibicininae with a revised diagnosis.