skip to main content

Title: Phylogeny of Membracoidea (Hemiptera: Auchenorrhyncha) based on transcriptome data

The suborder Auchenorrhyncha (“true hoppers”) comprises nearly half of known Hemiptera, with >43,000 known species of sap‐sucking herbivores distributed worldwide, including many important agricultural pests and vectors of plant disease. More than half of the known Auchenorrhyncha belong to superfamily Membracoidea (leaf‐ and treehoppers), which has been a source of phylogenetic contention for many years. To construct an improved backbone phylogeny of this superfamily, we obtained transcriptome data for multiple representatives of all 5 previously established extant families and nearly all subfamilies to test their monophyly and relationships. 138 taxa (132 Membracoidea and 6 outgroups) were sampled with an emphasis on families Cicadellidae and Membracidae, which were paraphyletic as previously defined by most authors, several problematic subfamilies (Aphrodinae, Eurymelinae, Ledrinae, Nicomiinae, Stegaspidinae and Tartessinae). We analysed different combinations of data sets (amino acid, complete nucleotide and degeneracy‐coded nucleotide) using different modelling schemes. The resultant trees based on different analyses are congruent in most nodes. Discordant nodes mainly pertain to relationships among cicadellid subfamilies and tribal relationships within Aphrodinae and Eurymelinae. Analyses of gene‐ and site concordance factors and quartet scores indicate that this instability is largely attributable to an overall lack of informative characters across genes and sites rather than strongly supported conflict among genes. According to the congruent nodes, we make the following revisions: combine Stegaspidinae and Centrotinae into a single subfamily, Centrotinae sensu lato; restore Stenocotini from Tartessinae to its original position in the Ledrinae; and transformHoldgatiellaEvans from Nicomiinae to Melizoderinae. In addition, to solve the paraphyly of both Cicadellidae and Membracidae, a preferred option would be to combine all five previously recognized families into a single family, Membracidae sensu lato; the other option could be to render Cicadellidae monophyletic by excluding Megophthalminae and Ulopinae from Cicadellidae and elevating them to status as separate families.

more » « less
Award ID(s):
Author(s) / Creator(s):
 ;  ;  ;  
Publisher / Repository:
Date Published:
Journal Name:
Systematic Entomology
Page Range / eLocation ID:
p. 97-110
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    The frenulum is a wing coupling structure that is found on the wings of most families of Lepidoptera. It is a single bristle or set of bristles that originate from the base of the hindwing that often interlocks with the forewing during flight. This wing coupling mechanism is thought to have been a major evolutionary innovation that allowed for enhanced flight in Lepidoptera. The sack‐bearer moths (Mimallonidae) are unusual among Lepidoptera in that not all species within the family have a frenulum. We test the hypothesis that the frenulum is not necessary and is therefore lost in mimallonids that have longer male forewings, because such wings are perhaps better suited to be coupled by other means. To understand the evolution of the frenulum, we inferred the most taxonomically and genetically sampled anchored hybrid enrichment‐based phylogeny of Mimallonidae, including 604 loci from all 41 genera and from 120 species, covering about 40% of the described species in the family. The maximum likelihood tree robustly supports major relationships within the family, and ancestral state reconstruction clearly recovers the frenulum as the plesiomorphic condition in Mimallonidae. Our results show that the frenulum is more often observed in species that have shorter, rather than longer, male forewings. The frenulum has historically been used as an important character for intrafamilial classification in Mimallonidae, but our results conclusively show that this character system is more variable than previously thought. Based on our results, we erect two new subfamilies, Roelofinae St Laurent & Kawahara,subfam.n.and Meneviinae St Laurent, Herbin, & Kawahara,subfam.n., for four genera previously consideredincertae sedis.In the predominantly frenulum‐lacking clade Cicinninae, we describe a new genus,CerradocinnusSt Laurent, Mielke, & Kawahara,gen.n., and the genusGonogrammastat. revalidated to include many species previously placed inCicinnussensu lato. With these changes,Cicinnuscan now be considered monophyletic. Thirty‐three species are transferred toGonogrammafromCicinnussensu lato.

    This published work has been registered on Zoobank,‐DA6A‐4814‐A312‐36CBAA168B8B.

    more » « less
  2. Abstract

    The Calyptratae, one of the most species‐rich fly clades, only originated and diversified after the Cretaceous–Palaeogene extinction event and yet exhibit high species diversity and a diverse array of life history strategies including predation, phytophagy, saprophagy, haematophagy and parasitism. We present the first phylogenomic analysis of calyptrate relationships. The analysis is based on 40 species representing all calyptrate families and on nucleotide and amino acid data for 1456 single‐copy protein‐coding genes obtained from shotgun sequencing of transcriptomes. Topologies are overall well resolved, robust and largely congruent across trees obtained with different approaches (maximum parsimony, maximum likelihood, coalescent‐based species tree, four‐cluster likelihood mapping). Many nodes have 100% bootstrap and jackknife support, but the true support varies by more than one order of magnitude [Bremer support from 3 to 3427; random addition concatenation analysis (RADICAL) gene concatenation size from 10 to 1456]. Analyses of a Dayhoff‐6 recoded amino acid dataset also support the robustness of many clades. The backbone topology Hippoboscoidea+(Fanniidae+(Muscidae+((Anthomyiidae–Scathophagidae)+Oestroidea))) is strongly supported and most families are monophyletic (exceptions: Anthomyiidae and Calliphoridae). The monotypic Ulurumyiidae is either alone or together with Mesembrinellidae as the sister group to the rest of Oestroidea. The Sarcophagidae are sister to Mystacinobiidae+Oestridae. Polleniinae emerge as sister group to Tachinidae and the monophyly of the clade Calliphorinae+Luciliinae is well supported, but the phylogenomic data cannot confidently place the remaining blowfly subfamilies (Helicoboscinae, Ameniinae, Chrysomyinae). Compared to hypotheses from the Sanger sequencing era, many clades within the muscoid grade are congruent but now have much higher support. Within much of Oestroidea, Sanger era and phylogenomic data struggle equally with regard to finding well‐supported hypotheses.

    more » « less
  3. Abstract

    The hemipteran suborder Auchenorrhyncha is a highly diverse, ecologically and agriculturally important group of primarily phytophagous insects which has been a source of phylogenetic contention for many years. Here, we have used transcriptome sequencing to assemble 2139 orthologues from 84 auchenorrhynchan species representing 27 families; this is the largest and most taxonomically comprehensive phylogenetic dataset for this group to date. We used both maximum likelihood and multispecies coalescent analyses to reconstruct the evolutionary history in this group using amino acid, nucleotide, and degeneracy‐coded nucleotide orthologue data. Although many relationships at the superfamily level were consistent between analyses, several differing, highly supported topologies were recovered using different datasets and reconstruction methods, most notably the differential placement of Cercopoidea as sister to either Cicadoidea or Membracoidea. To further interrogate the recovered topologies, we explored the contribution of genes as partitioned by third‐codon‐position guanine‐cytosine (GC) content and heterogeneity. We found consistent support for several relationships, including Cercopoidea + Cicadoidea, most often in genes that would be expected to be enriched for the true species tree if recombination‐based dynamics in GC content have contributed to the observed GC heterogeneity. Our results provide a generally well‐supported framework for future studies of auchenorrhynchan phylogeny and suggest that transcriptome sequencing is likely to be a fruitful source of phylogenetic data for resolving its clades. However, we caution that future work should account for the potential effects of GC content heterogeneity on relationships recovered in this group.

    more » « less
  4. Abstract

    The family Mutillidae (Hymenoptera) is a species‐rich group of aculeate wasps that occur worldwide. The higher‐level classification of the family has historically been controversial due, in part, to the extreme sexual dimorphism exhibited by these insects and their morphological similarity to other wasp taxa that also have apterous females. Modern hypotheses on the internal higher classification of Mutillidae have been exclusively based on morphology and, further, they include Myrmosinae as a mutillid subfamily. In contrast, several molecular‐based family‐level studies of Aculeata recovered Myrmosinae as a nonmutillid taxon. To test the validity of these morphology‐based classifications and the phylogenetic placement of the controversial taxon Myrmosinae, a phylogenomic study of Mutillidae was conducted using ultraconserved elements (UCEs). All currently recognized subfamilies and tribes of Mutillidae were represented in this study using 140 ingroup taxa. The maximum likelihood criterion (ML) and the maximum parsimony criterion (MP) were used to infer the phylogenetic relationships within the family and related taxa using an aligned data set of 238,764 characters; the topologies of these respective analyses were largely congruent. The modern higher classification of Mutillidae, based on morphology, is largely congruent with the phylogenomic results of this study at the subfamily level, whereas the tribal classification is poorly supported. The subfamily Myrmosinae was recovered as sister to Sapygidae in the ML analysis and sister to Sapygidae + Pompilidae in the MP analysis; it is consequently raised to the family level, Myrmosidae,stat.nov.The two constituent tribes of Myrmosidae are raised to the subfamily level, Kudakrumiinae,stat.nov., and Myrmosinae,stat.nov.All four recognized tribes of Mutillinae were found to be non‐monophyletic; three additional mutilline clades were recovered in addition to Ctenotillini, Mutillini, Smicromyrmini, and Trogaspidiini sensu stricto. Three new tribes are erected for members of these clades: Pristomutillini Waldren,trib.nov., Psammothermini Waldren,trib.nov., and Zeugomutillini Waldren,trib.nov.All three recognized tribes of Sphaeropthalminae were found to be non‐monophyletic; six additional sphaeropthalmine clades were recovered in addition to Dasymutillini, Pseudomethocini, and Sphaeropthalmini sensu stricto. The subtribe Ephutina of Mutillinae: Mutillini was found to be polyphyletic, with theEphutagenus‐group recovered within Sphaeropthalminae and theOdontomutillagenus‐group recovered as sister to Myrmillinae + Mutillinae. Consequently, the subtribe Ephutina is transferred from Mutillinae: Mutillini and is raised to a tribe within Sphaeropthalminae, Ephutini,stat.nov.Further, the taxon Odontomutillinae,stat.nov., is raised from a synonym of Ephutina to the subfamily level. The sphaeropthalmine tribe Pseudomethocini was found to be polyphyletic, with the subtribe Euspinoliina recovered as a separate clade in Sphaeropthalminae; consequently, Euspinoliina is raised to a tribe, Euspinoliini,stat.nov., in Sphaeropthalminae. The dasylabrine tribe Apteromutillini was recovered within Dasylabrini and is proposed as a new synonym of Dasylabrinae. Finally, dating analyses were conducted to infer the ages of the Pompiloidea families (Mutillidae, Myrmosidae, Pompilidae, and Sapygidae) and the ages of the Mutillidae subfamilies and tribes.

    more » « less
  5. Large systematic revisionary projects incorporating data for hundreds or thousands of taxa require an integrative approach, with a strong biodiversity-informatics core for efficient data management to facilitate research on the group. Our original biodiversity informatics platform, 3i (Internet-accessible Interactive Identification) combined a customized MS Access database backend with ASP-based web interfaces to support revisionary syntheses of several large genera of leafhopers (Hemiptera: Auchenorrhyncha: Cicadellidae). More recently, for our National Science Foundation sponsored project, “GoLife: Collaborative Research: Integrative genealogy, ecology and phenomics of deltocephaline leafhoppers (Hemiptera: Cicadellidae), and their microbial associates”, we selected the new open-source platform TaxonWorks as the cyberinfrastructure. In the scope of the project, the original “3i World Auchenorrhyncha Database” was imported into TaxonWorks. At the present time, TaxonWorks has many tools to automatically import nomenclature, citations, and specimen based collection data. At the time of the initial migration of the 3i database, many of those tools were still under development, and complexity of the data in the database required a custom migration script, which is still probably the most efficient solution for importing datasets with long development history. At the moment, the World Auchenorrhyncha Database comprehensively covers nomenclature of the group and includes data on 70 valid families, 6,816 valid genera, 47,064 valid species as well as synonymy and subsequent combinations (Fig. 1). In addition, many taxon records include the original citation, bibliography, type information, etymology, etc. The bibliography of the group includes 37,579 sources, about 1/3 of which are associated with PDF files. Species have distribution records, either derived from individual specimens or as country and state level asserted distribution, as well as biological associations indicating host plants, predators, and parasitoids. Observation matrices in TaxonWorks are designed to handle morphological data associated with taxa or specimens. The matrices may be used to automatically generate interactive identification keys and taxon descriptions. They can also be downloaded to be imported, for example, into Lucid builder, or to perform phylogenetic analysis using an external application. At the moment there are 36 matrices associated with the project. The observation matrix from GoLife project covers 798 taxa by 210 descriptors (most of which are qualitative multi-state morphological descriptors) (Fig. 2). Illustrations are provided for 9,886 taxa and organized in the specialized image matrix and could be used as a pictorial key for determination of species and taxa of a higher rank. For the phylogenetic analysis, a dataset was constructed for 730 terminal taxa and >160,000 nucleotide positions obtained using anchored hybrid enrichment of genomic DNA for a sample of leafhoppers from the subfamily Deltocephalinae and outgroups. The probe kit targets leafhopper genes, as well as some bacterial genes (endosymbionts and plant pathogens transmitted by leafhoppers). The maximum likelihood analyses of concatenated nucleotide and amino acid sequences as well as coalescent gene tree analysis yielded well-resolved phylogenetic trees (Cao et al. 2022). Raw sequence data have been uploaded to the Sequence Read Archive on GenBank. Occurrence and morphological data, as well as diagnostic images, for voucher specimens have been incorporated into TaxonWorks. Data in TaxonWorks could be exported in raw format, get accessed via Application Programming Interface (API), or be shared with external data aggregators like Catalogue of Life, GBIF, iDigBio. 
    more » « less