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The Mitochondrial Genome of a Stick Insect Extatosoma Tiaratum (Phasmatodea) and the Phylogeny of Polyneopteran Insects

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The Mitochondrial Genome of a Stick Insect Extatosoma Tiaratum (Phasmatodea) and the Phylogeny of Polyneopteran Insects Journal of Insect Biotechnology and Sericology 80, 79-88 (2011) The mitochondrial genome of a stick insect Extatosoma tiaratum (Phasmatodea) and the phylogeny of polyneopteran insects Shuichiro Tomita, Kenji Yukuhiro and Natuo Kômoto＊ National Institute of Agrobiological Sciences; Tsukuba, Ibaraki 305-8634, Japan (Received August 20, 2011; Accepted April 12, 2012) Polyneoptera is an assemblage of 11 insect orders consisting of lower neopteran insects. The interordinal rela- tionships within Polyneoptera remain highly controversial and ancient rapid radiations are thought to be respon- sible. Phasmatodea, whose phylogenetic position among Polyneoptera is quite unstable, has been thought to be a key taxon to resolve the polyneopteran phylogeny. We determined the full-length sequence of the mitochondrial genome of a stick insect, Extatosoma tiaratum, and explored the phylogeny of polyneopteran insects using nu- cleic acid as well as amino acid sequences from the mitogenome. Our analyses recovered a close relationship between Phasmatodea, Mantophasmatodea and Grylloblattodea. Dictyoptera was placed as a sister to this group. The monophyly of Orthoptera was confirmed and Plecoptera was placed as a sister group of this order. Six clades are recovered within Phasmatodea in this study and most of them challenge the conventional classifi- cation system. Key words: mitogenomics, molecular phylogeny, Polyneoptera Bradler, 2006), has also been placed as a sister to Plecop- INTRODUCTION tera, Dermaptera, or Zoraptera. Many previous studies Polyneoptera is a large group represented by 11 insect have found a close relationship between Orthoptera and orders including Blattodea (cockroaches), Dermaptera Phasmatodea (Kamp, 1973; Kukalová-Peck, 1991; Flook (earwigs), Embioptera (web-spinners), Grylloblattodea and Rowell, 1998; Wheeler et al., 2001; Terry and Whit- (ice-crawlers), Isoptera (termites), Mantodea (praying ing, 2005). However, the specialized state of sperm ultra- mantises), Mantophasmatodea (heel-walkers), Phasmato- structure is shared with Dermaptera and Phasmatodea, dea (stick insects), Plecoptera (stoneflies), Orthoptera thus suggesting sister-group relationships among these or- (grasshoppers), and Zoraptera (angel insects). Because the ders (Jamieson, 1987). derived states of morphologic characteristics have a mark- Previous studies have demonstrated that the mitochon- edly sporadic distribution among these orders, their rela- drial genome provides useful information when perform- tionships to each other and to the Paraneoptera and ing phylogenetic analyses (Boore and Brown, 1998; Endopterygota remain unclarified. In addition, because the Lavrov and Lang, 2005). Several convenient features of monophyly of Polyneoptera has not been well established, the mitogenome can be used to infer its phylogeny, such Kristensen et al. (1991) avoided the use of the word as its cellular abundance, the absence of recombination, “Polyneoptera” and instead referred to them as “the lower and the unambiguous orthology of genes, although lin- Neoptera”. Nevertheless, many hypotheses have been sug- eage-specific compositional heterogeneity and accelerated gested to explain the interordinal relationships of Polyne- substitution rates are major factors that negatively affect optera. Only the monophyly of Dictyoptera (Mantodea+ mitochondrial phylogenies. Blattodea+Isoptera) (Inward et al., 2007) and the sister re- In this work, we identified the full-length mitochondrial lationship of Grylloblattodea+Mantophasmatodea (Xenon- genome sequence of a stick insect, Extatosoma tiaratum, omia) (Terry and Whiting, 2005; cf. Plazzi et al., 2011) which inhabits in Queensland and New South Wales, Aus- have been repeatedly recovered by various molecular and tralia (Gurney, 1947). Also, we explored phasmatodean morphological studies (Arillo and Engel, 2006; Kjer et al., and polyneopteran phylogenetics using the most thorough 2006; Ishiwata et al., 2011). species sampling of mitochondrial genomes to date. Among polyneopteroid orders, the phylogenetic place- ment of Phasmatodea is extraordinarily unstable; it has MATERIALS AND METHODS been hypothesized to be a sister group to most orders within Polyneoptera. Embioptera, the most favored sister DNA extraction and sequencing group in recent years (Beutel and Gorb, 2001; Klug and Total genomic DNA was extracted from eggs using common methods (Sambrook et al., 1989). The eggs were *To whom correspondence should be addressed. laid by a female obtained from a pet shop and the speci- Fax: +81-29-838-6263. Tel: +81-29-838-6285. men of the female individual is maintained as the voucher Email: [email protected] in our laboratory. PCR amplification and the mitochondri- 80 Tomita et al. al genome sequencing strategy were performed as de- al., 2011) as previously described (Kômoto et al., 2011). scribed previously (Kômoto et al., 2011). The sequence of In brief, we aligned the nucleotide sequences of mito- the Extatosoma tiaratum mitochondrial genome, which chondrial protein-coding genes (PCGs) based on their was identified in this study, was deposited in DDBJ with translated amino acid sequences, and rRNA genes were the accession number AB642680. aligned using MUSCLE (Edgar, 2004) in MEGA5. All aligned sets of PCGs and rRNA genes were concatenated Data set preparation and model finding for use in subsequent phylogenetic analyses. The list of Gene identification and alignment was performed using the species used in this study is shown in Table 1. Among ClustalW (Thompson et al., 1994) in MEGA5 (Tamura et them, two Odonata species, Davidius lunatus and Euphaea Table 1. Species used in this study Order Species accession No. Odonata Davidius lunatus* EU591677 Euphaea formosa* HM126547 Plecoptera Pteronarcys princeps AY687866 Mantodea Tamolanica tamolana DQ241797 Blattaria Blattella germanica EU854321 Eupolyphaga sinensis FJ830540 Periplaneta fuliginosa AB126004 Isoptera Reticulitermes flavipes EF206314 Reticulitermes virginicus EF206318 Grylloblattodea Grylloblatta sculleni DQ241796 Mantophasmatodea Sclerophasma paresisense DQ241798 Phasmatodea: Timematodea Timema californicum DQ241799 Phasmatodea: Verophasmatodea Bacillus atticus GU001955 Bacillus rossius GU001956 Entoria okinawaensis AB477459 Extatosoma tiaratum AB642680 Heteropteryx dilatata AB477468 Megacrania alpheus AB477471 Micadina phluctainoides AB477466 Neohirasea japonica AB477469 Orestes mouhotii AB477462 Phyllium giganteum AB477461 Phraortes illepidus AB477460 Phraortes sp. (Miyako Is.) AB477465 Phraortes sp. (Iriomote Is.) AB477464 Phobaeticus serratipes AB477467 Ramulus hainanense FJ156750 Ramulus irregulariterdentatus AB477463 Sipyloidea sipylus AB477470 Orthoptera: Ensifera Anabrus simplex EF373911 Deracantha onos EU137664 Elimaea cheni GU323362 Gampsocleis gratiosa EU527333 Gryllotalpa orientalis AY660929 Myrmecophilus manni EU938370 Ruspolia dubia EF583824 Troglophilus neglectus EU938374 Orthoptera: Caelifera Acrida willemsei EU938372 Atractomorpha sinensis EU263919 Ellipes minuta GU945502 Euchorthippus fusigeniculatus HM583652 Gomphocerus licenti GQ180102 Locusta migratoria X80245 Oedaleus decorus EU513374 Schistocerca gregaria GQ491031 * outgroup taxa Polyneopteran phylogeny based on mitogenome 81 formosa, were used as the outgroup taxa. We constructed burn-in and combined the resulting MCMC tree samples nucleotide data sets composed of 11,621 nucleotide sites for subsequent estimation of posteriors. For amino acid from 13 concatenated mitochondrial PCGs and two rRNA data sets, we ran four concurrent analyses with eight genes (nt123). We also made a nucleotide data set exclud- chains each for 1.4 × 107 generations and discarded the ing the third codon position of the PCGs, which was com- first 70,000 samplings as burn-in. We conducted ML anal- posed of 8,162 sites. Amino acid data sets consisting of yses using RAxML PTHREADS 7.2.8 (Stamatakis, 2006). 3,459 sites were derived from the 13 PCGs. We applied ML tree searches and rapid bootstrapping We used Kakusan4 (Tanabe, 2011) to find nucleotide within one step (1,000 bootstrap replicates). RAxML used substitution models and partitioning strategies for the nu- randomized maximum parsimony starting trees for both cleotide data sets. Breaking down the nucleotide data by nucleotide and amino acid data sets. codon positions within each gene resulted in 41 partitions (first, second, and third codon positions for each of the 13 Topology test PCGs, rrnS, and rrnL) for the full nucleotide data set The tree topologies were statistically tested using Tree- (nt123 data set) and 28 partitions for the data set, exclud- Puzzle 5.2 (Schmidt et al., 2002) and CONSEL v. 0.1i, ing the third codon positions (nt12 data set), which were which perform the Kishino-Hasegawa (KH), Shimodaira- chosen for both Bayesian and maximum likelihood (ML) Hasegawa (SH), and approximately unbiased (AU) tests analyses. The likelihood was calculated based on the se- (Kishino and Hasegawa, 1989; Shimodaira and Hasegawa, quences separated into each codon position of each PCG. 1999, 2001; Shimodaira, 2002). Alternative topologies that Finally, a nucleotide substitution model was selected us- were tested were hypothesized based on the unstable ing the number of sites as the sample size based on the branching in the present analyses. Bayesian information criterion (BIC) for Bayesian analy- ses and Akaike’s information criterion (AIC) for ML anal- Substitution saturation test yses. Because Kakusan4 selects a nucleotide substitution We evaluated the level
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