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This Article Appeared in a Journal Published by Elsevier. the Attached This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright Author's personal copy Gene 515 (2013) 349–358 Contents lists available at SciVerse ScienceDirect Gene journal homepage: www.elsevier.com/locate/gene The complete mitochondrial genome of Biston panterinaria (Lepidoptera: Geometridae), with phylogenetic utility of mitochondrial genome in the Lepidoptera Xiushuai Yang a,b, Dayong Xue a, Hongxiang Han a,⁎ a Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China b Graduate University of the Chinese Academy of Sciences, Beijing 100049, China article info abstract Article history: The complete mitochondrial genome (mitogenome) of the Chinese pistacia looper Biston panterinaria was Accepted 1 November 2012 sequenced and annotated (15,517 bp). It contains the typical 37 genes of animal mitogenomes and a high Available online 5 December 2012 A+T content (79.5%). All protein coding genes (PCGs) use standard ATN initiation codons except for cytochrome c oxidase 1 (COX1) with CGA. Eleven PCGs use a common stop codon of TAA or TAG, whereas COX2 and NADH Keywords: dehydrogenase 4 (ND4) use a single T. All transfer RNA (tRNA) genes have the typical clover-leaf structure with Mitochondrial genome the exception of tRNASer(AGN). We reconstructed a preliminary mitochondrial phylogeny of six ditrysian super- Biston panterinaria Molecular phylogeny families and performed comparative analyses of inference methods (Bayesian Inference (BI), Maximum Likeli- hood (ML), and Maximum Parsimony (MP)), dataset compositions (including and excluding 3rd codon positions), and alignment methods (Muscle, Clustal W, and MAFFT). Our analyses indicated that inference methods and dataset compositions more significantly affected the phylogenetic results than alignment methods. BI analysis consistently revealed uncontroversial relationships with all dataset compositions. By contrast, ML analysis failed to reconstruct stable phylogeny at two nodes, whereas MP analysis had more difficulties in the tree resolution and nodal support. Distinct from most previous studies, our analyses revealed that Geometroidea had a closer lineage relationship with Bombycoidea than Noctuoidea. Similar to previous molecular studies, our analyses revealed that Hesperiidae were nested in the Papilionoidea clade, providing further evidence to the previous concept that Papilionoidea was paraphyletic, and none of the butterflies were associated with the Macroheterocera. © 2012 Elsevier B.V. All rights reserved. 1. Introduction 2009b; Hao et al., 2012; Jiang et al., 2009; Kim et al., 2009b, 2011; Mahendran et al., 2006), mitogenomes are also important in various Mitochondrial genomes (mitogenomes) of insects are typically scientific disciplines, such as comparative and evolutionary genomics double-stranded and circular molecules that span 14–20 kb. They con- (Ballard, 2000; Ballard and Rand, 2005; Papanicolaou et al., 2008), tain 13 protein coding genes (PCGs), 2 ribosomal RNA (rRNA) genes, molecular evolution (Brower, 1994; Zakharov et al., 2004), phylo- and 22 transfer RNA (tRNA) genes (Boore, 1999; Wolstenholme, geography (Avise, 2000), and population genetics (Avise et al., 1987; 1992), as well as a non-coding region known as the A+T rich or control Hurst and Jiggins, 2005). region, which participates in the initiation of transcription and replica- Lepidoptera is one of the world largest insect orders, second only tion (Taanman, 1999; Zhang and Hewitt, 1997; Zhang et al., 1995). In to Coleoptera, with approximately 157,424 described species (van addition to their application in the reconstruction of phylogenetic rela- Nieukerken et al., 2011). The controversial issues of the phylogenetic re- tionships among insects (Cameron and Whiting, 2008; Dowton et al., lationships in the Lepidoptera have been intensively discussed, at both deep-level and low-level (Fibiger et al., 2010; Mutanen et al., 2010; Sihvonen et al., 2011; Wahlberg et al., 2005; Zahiri et al., 2011, 2012). Abbreviations: Mitogenome, mitochondrial genome; PCGs, protein coding genes; Increasing numbers of molecular markers have been exploited for phy- – ATP6 and ATP8, ATP synthase subunits 6 and 8 genes; COX1-3, cytochrome c oxidase 1 logenetic analyses. These markers include mitochondrial genes large 3genes;CYTB,cytochromeb gene; ND1-6 and ND4L, NADH dehydrogenase subunits 1–6 and 4L genes; rRNA, ribosomal RNA; lrRNA and srRNA, large and small subunit ribo- subunit ribosomal RNA (lrRNA) (Pashley and Ke, 1992), small subunit somal RNA; tRNA, transfer RNA; PCR, polymerase chain reaction; DHU, dihydrouridine; ribosomal RNA (srRNA) (Niehuis et al., 2006), cytochrome c oxidase 1 TΨC, pseudouridine; BI, Bayesian Inference; ML, Maximum Likelihood; MP, Maximum (COX1) (Wahlberg et al., 2005; Wu et al., 2010), COX2 (Braby et al., Parsimony; BP, bootstrap percentage. 2005), cytochrome b (CYTB) (Li et al., 2005), NADH dehydrogenase 1 ⁎ Corresponding author at: Key Laboratory of Zoological Systematics and Evolution, (ND1) (Martin and Pashley, 1992; Weller et al., 1994), and ND5 (Yagi Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China. Tel.: +86 10 64807230; fax: +86 10 64807099. et al., 1999), as well as the nuclear genes 18S (Weller et al., 1992), 28S E-mail address: [email protected] (H. Han). (Abraham et al., 2001), CAD (Regier et al., 2008b; Zwick, 2008), DDC 0378-1119/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.gene.2012.11.031 Author's personal copy 350 X. Yang et al. / Gene 515 (2013) 349–358 (Regier et al., 2001, 2002, 2005), EF-1α (Mitchell et al., 1997, 2006), Table 1 enolase (Regier et al., 2008a), GAPDH (Wahlberg and Wheat, 2008; Statistics of the data matrices in the study. Wahlberg et al., 2009), IDH (Sihvonen et al., 2011; Zwick et al., 2011), Dataset name Number of nucleotides (bp) MDH (Zahiri et al., 2011, 2012), RpS5 (Mutanen et al., 2010), and PCG12MU 7790 wingless (Kawahara et al., 2009). Molecular phylogenetic studies of PCG12CW 7748 the Lepidoptera used to rely on a combination of two or more of the PCG12MA 7740 aforementioned molecular markers, and different markers or different PCG123MU 11,685 taxon samplings result in inconsistencies (Heikkilä et al., 2012; PCG123CW 11,622 PCG123MA 11,650 Mitchell et al., 1997, 2006; Mutanen et al., 2010; Regier et al., 2009; Wahlberg et al., 2005; Weller et al., 1994; Zahiri et al., 2011). Recently, the expansion of molecular markers and taxon samplings in the Lepi- doptera, especially in the superfamilies Bombycoidea, Noctuoidea, and in July 2011. Three legs from one side of the body were removed Papilionoidea, has greatly improved the resolution of some ambiguous and preserved in 100% ethanol during collection. After transport to phylogenetic relationships (Heikkilä et al., 2012; Mutanen et al., 2010; the laboratory, the legs were stored at −20 °C until DNA extraction, Regier et al., 2009; Zahiri et al., 2011; Zwick et al., 2011). However, and the specimens were deposited at the Museum of the Institute of many relationships remain poorly resolved. Zoology, Chinese Academy of Sciences. Total genomic DNA was Considerable efforts have been expended in the past decade extracted from the leg muscle tissue using a Qiagen DNeasy Blood & to reconstruct the evolutionary relationships using mitogenomes Tissue Kit (69506). (Cameron et al., 2007, 2009; Dowton et al., 2009a; Fenn et al., 2008; Kawaguchi et al., 2001; Minegishi et al., 2005; Miya et al., 2003; 2.2. Polymerase chain reaction (PCR) amplification and sequencing Song et al., 2010; Wiegmann et al., 2011). A range of phylogenetic approaches such as inference methods, partitioning strategies, align- The entire genome was amplified using standard PCR methods with ment methods, and gene exclusion have been tested to find the most a set of universal primers for the lepidopteran mitogenome (Folmer appropriate methods for analyzing mitogenomes, especially in insects et al., 1994; Lee et al., 2006; Simon et al., 1994, 2006; Zhao et al., (Cameron et al., 2009; Dowton et al., 2009a; Fenn et al., 2008; Song 2011; Zhu et al., 2010). Then, perfectly matched primers for internal et al., 2010; Wiegmann et al., 2011). In these studies, three of the four fragments were designed based on the sequences amplified by the most diverse holometabolous insect orders (Coleoptera, Diptera, Lepi- universal primers. Short PCRs were performed using Takara Taq™ doptera, and Hymenoptera) have been examined (Cameron et al., DNA polymerase (DR001B) under the following cycling parameters: 2007; Dowton et al., 2009a; Song et al., 2010). The number of complete 94 °C for 2 min; 35 cycles of 30 s at 94 °C, 30 s at 53 °C, and 1 min at or nearly complete lepidopteran mitogenomes in the GenBank has rap- 72 °C; and 72 °C for 10 min. Long PCRs were performed using Takara idly increased to 138,
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