Molecular phylogeny of Cicadomorpha (Insecta: Hemiptera: Cicadoidea, Cercopoidea and Membracoidea): adding evidence to the controversy

Abstract.  The hemipteran infraorder Cicadomorpha comprises the superfamilies Cicadoidea (cicadas), Cercopoidea (spittlebugs or froghoppers) and Membracoidea (leafhoppers and treehoppers). Earlier attempts to determine relationships among these three monophyletic lineages using either morphological or molecular data suffered from insufficient sampling (taxonomic and data) and problematic tree rooting, leading to discordant results. Presented here are phylogenetic reconstructions within Cicadomorpha based on DNA nucleotide sequence data from multiple genetic markers (18S rDNA, 28S rDNA, and histone 3) sequenced from representative taxa of Cicadidae, Tettigarctidae, Cercopidae, Aphrophoridae, Clastopteridae, Machaerotidae, Epipygidae, Cicadellidae, Membracidae, Myerslopiidae and Aetalionidae. To test the robustness of the phylogenetic signal, these sequence data were analysed separately and in combination under various alignment parameters using both manual alignment (of both attenuated and full sequences) and alignment via clustal x. The results demonstrate clearly that, despite the alignment method used, basing a phylogeny on a single gene region is often misleading. Analyses of the combination of datasets support the major relationships within Cicadomorpha as (Membracoidea (Cicadoidea, Cercopoidea)). Internal relationships recovered within each superfamily shows evidence for: (1) the placement of Myerslopiidae as the sister group of the remaining Membracoidea; (2) the paraphyly of Cicadellidae; (3) the sister‐group relationship between Machaerotidae and Clastopteridae; (4) the monophyly of Cercopidae; (5) the diversification of Epipygidae from within the possibly paraphyletic Aphrophoridae.

[1]  Evolution of Cicadomorpha (Insecta, Hemiptera) , 2006 .

[2]  J. Cryan,et al.  Inferring a Phylogeny for Hemiptera: Falling into the 'Autapomorphic Trap' , 2006 .

[3]  M. Whiting,et al.  Treehopper trees: phylogeny of Membracidae (Hemiptera: Cicadomorpha: Membracoidea) based on molecules and morphology , 2004 .

[4]  N. Moran,et al.  Molecular phylogeny of the homoptera: a paraphyletic taxon , 1995, Journal of Molecular Evolution.

[5]  M. Whiting,et al.  The problem with “the Paleoptera Problem:” sense and sensitivity , 2003, Cladistics : the international journal of the Willi Hennig Society.

[6]  Memoirs of the American Entomological Institute , 2003 .

[7]  J. P. Duffels,et al.  Cladistic analysis and biogeography of the cicadas of the Indo‐Pacific subtribe Cosmopsaltriina (Hemiptera: Cicadoidea: Cicadidae) , 2002 .

[8]  M. Whiting.  Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera , 2002 .

[9]  M. Fletcher,et al.  Morphology of the antennal sensilla in four Australian spittlebug species (Hemiptera: Cercopidae) with implications for phylogeny , 2002 .

[10]  D. Swofford.  PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4.0b10 , 2002 .

[11]  R. Rakitov.  Structure and Function of the Malpighian Tubules, and Related Behaviors in Juvenile Cicadas: Evidence of Homology with Spittlebugs (Hemiptera: Cicadoidea & Cercopoidea) , 2002 .

[12]  M. Whiting.  Phylogeny of the holometabolous insect orders based on 18S ribosomal DNA: when bad things happen to good data. , 2002, EXS.

[13]  K. Hamilton.  A new family of froghoppers from the American tropics (Hemiptera: Cercopoidea: Epipygidae) , 2001 .

[14]  C. Dietrich,et al.  Morphology‐based phylogeny of the treehopper family Membracidae (Hemiptera: Cicadomorpha: Membracoidea) , 2001 .

[15]  C. Dietrich,et al.  Phylogeny of the major lineages of Membracoidea (Insecta: Hemiptera: Cicadomorpha) based on 28S rDNA sequences. , 2001, Molecular phylogenetics and evolution.

[16]  Hidetoshi Shimodaira,et al.  Evaluating hypotheses on the origin and evolution of the New Zealand alpine cicadas (Maoricicada) using multiple-comparison tests of tree topology. , 2001, Molecular biology and evolution.

[17]  K. Yoshizawa,et al.  Phylogenetic analysis of paraneopteran orders (Insecta: Neoptera) based on forewing base structure, with comments on monophyly of Auchenorrhyncha (Hemiptera) , 2001 .

[18]  C. Dietrich,et al.  Phylogeny of the treehoppers (Insecta: Hemiptera: Membracidae): evidence from two nuclear genes. , 2000, Molecular phylogenetics and evolution.

[19]  T. Bourgoin,et al.  18S rRNA secondary structure and phylogenetic position of Peloridiidae (Insecta, hemiptera). , 2000, Molecular phylogenetics and evolution.

[20]  C. Simon,et al.  The performance of several multiple-sequence alignment programs in relation to secondary-structure features for an rRNA sequence. , 2000, Molecular biology and evolution.

[21]  V. Thompson.  Spittlebugs associated with actinorhizal host plants , 1999 .

[22]  K. Andrew.  The ground-dwelling leafhoppers Myerslopiidae, new family, and Sagmatiini, new tribe (Homoptera : Membracoidea) , 1999 .

[23]  G. Edgecombe,et al.  Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution , 1998 .

[24]  J. Thompson,et al.  The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. , 1997, Nucleic acids research.

[25]  R DeSalle,et al.  Multiple sources of character information and the phylogeny of Hawaiian drosophilids. , 1997, Systematic biology.

[26]  W C Wheeler,et al.  The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. , 1997, Systematic biology.

[27]  J. T. Sorensen,et al.  Paraphyly of Homoptera and Auchenorrhyncha inferred from 18S rDNA nucleotide sequences , 1995 .

[28]  J. T. Sorensen,et al.  Non-monophyly of Auchenorrhyncha ("Homoptera"), based upon 18S rDNA phylogeny: eco-evolutionary and cladistic implications within pre-heteropterodea Hemiptera (s.l.) and a proposal for new monophyletic suborders , 1995 .

[29]  V. Thompson.  Spittlebug indicators of nitrogen‐fixing plants , 1994 .

[30]  C. Dietrich,et al.  Superfamily Membracoidea (Homoptera: Auchenorrhyncha). II. Cladistic analysis and conclusions , 1993 .

[31]  C. Dietrich,et al.  Superfamily Membracoidea (Homoptera: Auchenorrhyncha). I. Introduction and revised classification with new family‐group taxa , 1993 .

[32]  D. Shcherbakov.  The earliest leafhoppers (Hemiptera: Karajassidae n. fam.) from the Jurassic of Karatau , 1992 .

[33]  D. Hillis,et al.  Ribosomal DNA: Molecular Evolution and Phylogenetic Inference , 1991, The Quarterly Review of Biology.

[34]  John M. Hancock,et al.  Evolution of the secondary structures and compensatory mutations of the ribosomal RNAs of Drosophila melanogaster. , 1988, Molecular biology and evolution.

[35]  Keith Hamilton.  MORPHOLOGY AND EVOLUTION OF THE RHYNCHOTAN HEAD (INSECTA: HEMIPTERA, HOMOPTERA) , 1981, The Canadian Entomologist.

[36]  J. Evans,et al.  The phylogeny of the Homoptera , 1963 .

[37]  The 270 Million Year History of Auchenorrhyncha (Homoptera) , 2022 .