Based on Mitochondrial Genomes
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See discussions, stats, and author profiles for this publication at: http://www.researchgate.net/publication/236260264 Phylogenomics of Hemiptera (Insecta: Paraneoptera) based on mitochondrial genomes ARTICLE in SYSTEMATIC ENTOMOLOGY · JANUARY 2013 Impact Factor: 2.55 · DOI: 10.1111/j.1365-3113.2012.00660.x CITATIONS DOWNLOADS VIEWS 8 74 130 9 AUTHORS, INCLUDING: Qiang Xie Jianfu Zhou Nankai University Dartmouth College 18 PUBLICATIONS 285 CITATIONS 6 PUBLICATIONS 36 CITATIONS SEE PROFILE SEE PROFILE Xiaoguang Liu Wenjun Bu Nankai Univrsity Nankai University 62 PUBLICATIONS 118 CITATIONS 44 PUBLICATIONS 340 CITATIONS SEE PROFILE SEE PROFILE Available from: Kai Dang Retrieved on: 17 August 2015 Systematic Entomology (2013), 38, 233–245 DOI: 10.1111/j.1365-3113.2012.00660.x Phylogenomics of Hemiptera (Insecta: Paraneoptera) based on mitochondrial genomes ∗ ∗ ∗ YING CUI1 , QIANG XIE1 ,JIMENGHUA1 , KAI DANG1, JIANFU ZHOU2, XIAOGUANG LIU2, GANG WANG2,XINYU1 and W E N J U N B U1 1Institute of Entomology, College of Life Sciences, Nankai University, Tianjin, China and 2College of Information Technical Science, Nankai University, Tianjin, China Abstract. Hemiptera is the largest order in Paraneoptera and the fifth largest in Insecta. Disputes about hemipteran phylogeny have concerned the monophyly of Auchenorrhyncha and relationships between the suborders Fulgoromorpha, Cicado- morpha, Coleorrhyncha and Heteroptera. In a phylogenomic study of Hemiptera, we add two new mitochondrial genomes of Peloridiidae (Coleorrhyncha) to those reported in GenBank, to complete the taxon sampling of all suborders. We used two types of data – amino acid sequences and nucleotides of various combinations between protein coding genes, tRNAs and rRNAs – to infer the phylogeny of Hemiptera. In total 27 taxa of Paraneoptera were sampled, 24 of them being hemipterans. Bayesian infer- ence, maximum likelihood and maximum parsimony analyses were employed. The relationship of Cicadomorpha + Heteroptera is always stable in the results with dif- ferent combinations between data types and phylogenetic methods, but our results challenge the monophyly of ‘Homoptera’ and Auchenorrhyncha. In evaluating the rel- ative contribution of each gene, the phylograms generated by single genes CO1, ND1, ND2, ND4 and ND5, respectively, closely matched the tree yielded by the combined datasets. In light of the taxon-sampling sensitivity of trees based on mitochondrial genomes, the results need to be tested with further data from nuclear genes. Introduction accepted since the 1960s to the present (Hennig, 1969; Carver et al., 1991; Kristensen, 1991; Yoshizawa & Saigusa, 2001). Hemiptera (true bugs) and Homoptera (planthoppers, leafhop- In this study, Hemiptera is used to mean Hemiptera (s.l.). pers, treehoppers, cicadas, spittlebugs, aphids, psyllids, scales, Different views of hemipteran phylogeny are summarized whiteflies, etc.) were established originally by Linnaeus (1758) in Fig. 1. Traditionally, no matter whether ‘Homoptera’ is according to features of the wing. Although merged into Ryn- regarded as a distinct order or as a suborder of Hemiptera, it gota in 1775 by Fabricius (modified to Rhynchota by Burmeis- consists of Sternorrhyncha and Auchenorrhyncha. Sternorrhyn- ter in 1835) based on the mouthpart structure, they were still cha was supported as a sister group to all the other hemipterans, treated as two separate orders until the 1930s (e.g. Brues & and named Euhemiptera (Zrzavy,´ 1990), by numerous phy- Melander, 1932), except by Latreille (1810) who recognized logenetic studies based on morphological evidence (Hennig, Heteroptera and ‘Homoptera’ as two sections of his order 1969, 1981; Kristensen, 1975, 1991; Schuh, 1979; Popov, Hemiptera (s.l.). The concept of Hemiptera (s.l.)hasbeen 1981; Minet & Bourgoin, 1986; Wootton & Betts, 1986; Correspondence: Wenjun Bu, Institute of Entomology, College of Zrzavy,´ 1990, 1992) and molecular evidence (Wheeler et al., Life Sciences, Nankai University, Weijin Road No. 94, Tianjin 300071, 1993; Campbell et al., 1994, 1995; Sorensen et al., 1995; China. E-mail: [email protected] von Dohlen & Moran, 1995; Ouvrard et al., 2000; Cryan & Urban, 2012). However, Homoptera has been argued to ∗These authors contributed equally to this work. be monophyletic based on evidence from the mitochondrial © 2012 The Royal Entomological Society 233 234 Y. Cui et al. genomes (mitogenomes), and thus the controversy over the characteristics (Shcherbakov, 1988; Zrzavy,´ 1990, 1992; Popov monophyly of Homoptera was revived (Song et al., 2010). & Shcherbakov, 1991, 1996; D’Urso, 1993; Grimaldi & Engel, Auchenorrhyncha traditionally has been divided into Fulgo- 2005). Although Shcherbakov (1988) regarded the extant romorpha and Cicadomorpha (Grimaldi & Engel, 2005). As to cicadomorphs and heteropterans as descendants of a common the monophyly of Auchenorrhyncha, both the molecular evi- ancestor, Popov & Shcherbakov (1991, 1996) argued that dence and the morphological evidence has been controversial Coleorrhyncha and Heteroptera did not have an immediate (Fig. 1). In fact, the nonmonophyletic view of Auchenorrhyn- common ancestor and were descended independently from cha includes different opinions. According to one hypothe- separate lineages. Hence, the phylogenetic relationships among sis, Fulgoromorpha rather than Cicadomorpha is more closely the higher-level hemipteran lineages remain unclear (Fig. 1). related to Heteroptera (Goodchild, 1966; Bourgoin, 1988, Mitogenomes have been used successfully to reconstruct 1993; Campbell et al., 1994; von Dohlen & Moran, 1995) or the phylogenetic relationships within some orders of Insecta Heteropterodea (Campbell et al., 1995; Sorensen et al., 1995). (Cameron et al., 2007, 2008; Fenn et al., 2008; Hua et al., In an alternative hypothesis, Cicadomorpha is placed as a sis- 2008, 2009; Wei et al., 2010). Until now, the mitogenomes ter group to Heteropterodea based on 18S rDNA (Ouvrard of four of the five hemipteran suborders – Sternorrhyncha, et al., 2000; Xie et al., 2008). Hamilton (1981) proposed that Cicadomorpha, Fulgoromorpha and Heteroptera – have been Cicadomorpha was sister group to Sternorrhyncha. reported in GenBank, which leaves the corresponding data for Coleorrhyncha, proposed originally by Myers & China Coleorrhyncha blank. Restricted distribution, small individual (1929), are small bugs with a crptic lifestyle. They possess size and secluded lifestyle may all make it hard to provide a mixture of cicadomorphan and bug-like characters (Bechly complete mitogenomic sequences for Coleorrhyncha. How- & Szwedo, 2007), and represent a separate suborder within ever, without the mitogenomic sequences of Coleorrhyncha, Hemiptera. This suborder includes a single extant family, phylogenomic sampling of Hemiptera are incomplete. Here we Peloridiidae, which is distributed now only in Patagonia included two mitogenomes of Coleorrhyncha and reconstructed and the Australian continent (Burckhardt et al., 2011). Its the higher-level phylogenomic relationships of Hemiptera with complete subordinal sampling for the first time. phylogenetic position within Hemiptera has long fascinated hemipterists. Peloridiids were placed first in Heteroptera (Breddin, 1897), but transferred to a suborder of their own Materials and methods (China, 1924) or included in the ‘Homoptera’ (Myers & China, 1929; China, 1962; Evans, 1963). Peloridiidae and Heteroptera Taxon sampling were treated as sister groups by Schlee (1969) but Cobben (1978) considered Schlee’s synapomorphies as superficial. Twenty-seven taxa were sampled in this study. Twenty- Although the close relationship between Peloridiidae and four of these were ingroups, which included all five suborders Heteroptera has been supported consistently by nuclear rDNAs of Hemiptera. Among them, the mitogenomes of Xenophyes (Campbell et al., 1995; Sorensen et al., 1995; Ouvrard et al., cascus Bergroth and Hackeriella veitchi (Hacker) are reported 2000; Xie et al., 2008; Cryan & Urban, 2012), controversies here for the first time. The remaining outgroups were sampled remain from the view of morphological and paleontological from Phthiraptera and Thysanoptera (Table 1). Fig. 1. The summarized phylogenetic relationships among the higher-level hemipteran lineages. © 2012 The Royal Entomological Society, Systematic Entomology, 38, 233–245 Phylogenomics of Hemiptera 235 ◦ Table 1. Hemipteran taxon sampling and the accession numbers of initial denaturation at 94 C, 32 cycles of 20 s denaturation at ◦ ◦ the corresponding mitogenomes. 94 C, 1 min annealing at 47–60 C and 1–10 mins elongation ◦ at 72 C depending on the size of products, and a final Taxa Accession number ◦ elongation for 10 min at 72 C. The primers used in this study Phthiraptera — are listed in File S1 and the specific primers named with the Bothriometopus macrocnemis NC_009983 first three letters ‘Xen’ were used for amplifying the sequences Campanulotes bidentatus compar NC_007884 of Xenophyes cascus and ‘Hac’ for Hackeriella veitchi. Thysanoptera — The PCR products were electrophoresed in 0.7–1% agarose Thrips imaginis NC_004371 gel and then purified. All the products were sequenced directly Hemiptera — Sternorrhyncha — in double directions by primer walking. Those fragments which Aleurochiton aceris NC_006160 failed direct sequencing were cloned into TA-cloning vector Aleurodicus dugesii NC_005939 pMD-18T (TaKaRa) and transformed into competent E. coli Acyrthosiphon pisum NC_011594 DH5α. Putative clones containing the PCR fragments