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The complete mitochondrial genome of Vanessa indica and phylogenetic analyses of the family Nymphalidae

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Abstract

Vanessa indica is a small butterfly lacking historical molecular and biological research. Vanessa indica belongs to the family Nymphalidae (Lepidoptera: Papilionoidea), which is the largest group of butterflies and are nearly ubiquitous. However, after more than a century of taxonomic and molecular studies, there is no consensus for family classification, and the phylogenetic relationships within Nymphalidae are controversial. The first objective was to sequence and characterize the complete mitochondrial genome of V. indica. The most important objective was to completely reconstruct the phylogenetic relationships for family members within Nymphalidae. The mitochondrial genomic DNA (mtDNA) of V. indica was extracted and amplified by polymerase chain reaction. The complete mitochondrial sequence was annotated and characterized by analyzing sequences with SeqMan program. The phylogenetic analyses were conducted on thirteen protein coding genes (PCGs) in 95 mtDNA of Nymphalidae downloaded from GenBank for reference using the maximum likelihood method and Bayesian inference to ensure the validity of the results. The complete mitogenome was a circular molecule with 15,191 bp consisting of 13 protein coding genes, two ribosomal RNA genes (16S rRNA and 12S rRNA), 22 transfer RNA (tRNA) genes, and an A + T-rich region (D-loop). The nucleotide composition of the genome was highly biased for A + T content, which accounts for 80.0% of the nucleotides. All the tRNAs have putative secondary structures that are characteristic of mitochondrial tRNAs, except tRNA Ser(AGN) . All the PCGs started with ATN codons, except cytochrome c oxidase subunit 1 (COX1), which was found to start with an unusual CGA codon. Four genes were observed to have unusual codons: COX1 terminated with atypical TT and the other three genes terminated with a single T. The A + T rich region of 327 bp consisted of repetitive sequences, including a ATAGA motif, a 19-bp poly-T stretch, and two microsatellite-like regions (TA)8. The phylogenetic analyses consistently placed Biblidinae as a sister cluster to Heliconiinae and Calinaginae as a sister clade to Satyrinae. Moreover, the phylogenetic tree identified Libytheinae as a monophyletic group within Nymphalidae. The complete mitogenome of V. indica was 15,191 bp with mitochondrial characterizations common for lepidopteran species, which enriched the mitochondria data of Nymphalid species. And the phylogenetic analysis revealed different classifications and relationships than those previously described. Our results are significant because they would be useful in further understanding of the evolutionary biology of Nymphalidae.

Keywords

Vanessa indica Mitochondrial genome Nymphalidae Phylogenetic analyses 

Notes

Acknowledgements

We wish to express our appreciations to Yun-he Wu, University of China Academy of Science, Wen-bo Li, Anhui University, for assistance during the experiment, corrections and comments regarding this manuscript. This study was sponsored by the Undergraduate student innovation and entrepreneurship training projects of Anhui University (J10118516034). The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.

Compliance with ethical standards

Conflict of interest

Youxue Lu declares that she has no conflict of interest. Naiyi Liu declares that she has no conflict of interest. Liuxiang Xu declares that he has no conflict of interest. Jie Fang declares that he has no conflict of interest. Shuyan Wang declares that she has no conflict of interest.

Ethical approval

The article does not contain any studies with human subjects or animals performed by any of the authors.

Supplementary material

13258_2018_709_MOESM1_ESM.docx (16 kb)
Supplementary material 1 (DOCX 15 KB)

References

  1. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723CrossRefGoogle Scholar
  2. Arunkumar KP, Metta M, Nagaraju J (2006) Molecular phylogeny of silkmoths reveals the origin of domesticated silkmoth, Bombyx mori from Chinese Bombyx mandarina and paternal inheritance of Antheraea proylei mitochondrial DNA. Mol Phylogenet Evol 40:419–427CrossRefPubMedGoogle Scholar
  3. Boore JL (1999) Animal mitochondrial genomes. Nucleic Acids Res 27:1767–1780CrossRefPubMedPubMedCentralGoogle Scholar
  4. Boore JL (2000) The duplication/random loss model for gene rearrangement exemplified by mitochondrial genomes of deuterostome animals. In: Sankoff D, Nadeau JH (eds) Comparative genomics. Kluwer Academic Publishers, Dordrecht, pp 133–216CrossRefGoogle Scholar
  5. Brower AV (2000) Phylogenetic relationships among the Nymphalidae (Lepidoptera) inferred from partial sequences of the wingless gene. Proc R Soc Lond B: Biol Sci 267:1201–1211CrossRefGoogle Scholar
  6. Cameron SL (2014) Insect mitochondrial genomics: implications for evolution and phylogeny. Annu Rev Entomol 59:95–117CrossRefPubMedGoogle Scholar
  7. Cameron SL, Whiting MF (2008) The complete mitochondrial genome of the tobacco hornworm, Manduca sexta (Insecta: Lepidoptera: Sphingidae), and an examination of mitochondrial gene variability within butterflies and moths. Gene 408:112–113CrossRefPubMedGoogle Scholar
  8. Chai HN, Du YZ, Zha BP (2012) Characterization of the complete mitochondrial genomes of Cnaphalocrocis medinalis and Chilo suppressalis (Lepidoptera: Pyralidae). Int J Biol Sci 8:561–579CrossRefPubMedPubMedCentralGoogle Scholar
  9. Chen MM, Li Y, Chen M, Wang H, Li Q, Xia RX, Zeng CY, Li YP, Liu YQ, Qin L (2014) Complete mitochondrial genome of the atlas moth, Attacus atlas (Lepidoptera: Saturniidae) and the phylogenetic relationship of Saturniidae species. Gene 545:95–101CrossRefPubMedGoogle Scholar
  10. Cheng XF, Zhang LP, Yu DN, Storey KB, Zhang JY (2016) The complete mitochondrial genomes of four cockroaches (Insecta: Blattodea) and phylogenetic analyses within cockroaches. Gene 586:115–122CrossRefPubMedGoogle Scholar
  11. Chou I (1994) Monograph of Chinese butterflies (in Chinese). Henan Scientific and Technological Publishing House, ZhengzhouGoogle Scholar
  12. Chou I (1998) Classification and identification of Chinese butterflies (in Chinese). Henan Scientific and Technological Publishing House, ZhengzhouGoogle Scholar
  13. Fan C, Xu C, Li JL, Lei Y, Gao Y, Xu CR, Wang RJ (2016) Complete mitochondrial genome of a satyrid butterfly, Ninguta schrenkii (Lepidoptera: Nymphalidae). Mitochondrial DNA A DNA Mapp Seq Anal 27: 80–81CrossRefPubMedGoogle Scholar
  14. Freitas AVL, Brown KS, Schultz T (2004) Phylogeny of the Nymphalidae (Lepidoptera). Syst Biol 53:363–383CrossRefPubMedGoogle Scholar
  15. Hao JS, Sun QQ, Zhao HB, Sun XY, Gai YH, Yang Q (2012) The complete mitochondrial genome of Ctenoptilum vasava (Lepidoptera: Hesperiidae: Pyrginae) and its phylogenetic implication. Comp Funct Genom 2012:1–13CrossRefGoogle Scholar
  16. Hassasin A, Léger N, Deutsch J (2005) Evidence for multiple reversals of asymmetric mutational constraints during the evolution of the mitochondrial genome of metazoan, and consequences for phylogenetic inferences. Syst Biol 54:277–298CrossRefGoogle Scholar
  17. Huang ZH, Dai PF, Zhao GF (2016) The complete mitochondrial genome of Heliconius pachinus (Insecta: Lepidoptera: Nymphalidae). Mitochondrial DNA A DNA Mapp Seq Anal 27:1251–1252CrossRefPubMedGoogle Scholar
  18. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755CrossRefPubMedGoogle Scholar
  19. Jiang ST (2009) Characterization of the complete mitochondrial genome of the giant silkworm moth, Eriogyna pyretorum (Lepidoptera: Saturniidae). Int J Biol Sci 5:351–365CrossRefPubMedPubMedCentralGoogle Scholar
  20. Kambhampati S, Smith PT (1995) PCR primers for the amplification of four insect mitochondrial gene fragments. Insect Mol Biol 4:233–236CrossRefPubMedGoogle Scholar
  21. Kang XC, Hu YQ, Hu J, Hu LQ, Wang F, Liu DB (2017) The mitochondrial genome of the lepidopteran host cadaver (Thitarodes sp.) of Ophiocordyceps sinensis and related phylogenetic analysis. Gene 598:32–42CrossRefPubMedGoogle Scholar
  22. Kawahara AY (2009) Phylogeny of snout butterflies (Lepidoptera: Nymphalidae: Libytheinae): combining evidence from the morphology of extant, fossil, and recently extinct taxa. Cladistics 25:263–278CrossRefGoogle Scholar
  23. Kim MJ, Kang AR, Jeong HC, Kim KG, Kim I (2011) Reconstructing intraordinal relationships in Lepidoptera using mitochondrial genome data with the description of two newly sequenced lycaenids, Spindasis takanonis and Protantigius superans (Lepidoptera: Lycaenidae). Mol Phylogenet Evol 61:436–445CrossRefPubMedGoogle Scholar
  24. Lavrov DV, Brown WM, Boore JL (2000) A novel type of RNA editing occurs in the mitochondrial tRNAs of the centipede Lithobius forficatus. Proc Natl Acad Sci USA 97:13738–13742CrossRefPubMedPubMedCentralGoogle Scholar
  25. Li CL, Zhu BY (1992) The profile of butterflies in China (in Chinese). Shanghai Yuandong Press, ShanghaiGoogle Scholar
  26. Liu Y, Li Y, Pan M, Dai F, Zhu X, Lu C, Xiang Z (2008) The complete mitochondrial genome of the Chinese oak silkmoth, Antheraea pernyi (Lepidoptera: Saturniidae). Acta Biochim et Biophys Sin 40:693–703CrossRefGoogle Scholar
  27. Liu QN, Zhu BJ, Dai LS, Wei GQ, Liu CL (2012) The complete mitochondrial genome of the wild silkworm moth, Actias selene. Gene 505:291–299CrossRefPubMedGoogle Scholar
  28. Liu NY, Li N, Yang PY, Sun CQ, Fang J, Wang SY (2017a) The complete mitochondrial genome of Damora sagana and phylogenetic analyses of the family Nymphalidae. Genes Genom.  https://doi.org/10.1007/s13258-017-0614-8 Google Scholar
  29. Liu QN, Xin ZZ, Zhu XY, Chai XY, Zhao XM, Zhou CL, Tang BP (2017b) A transfer RNA gene rearrangement in the lepidopteran mitochondrial genome. Biochem Biophys Res Commun 489:149–154CrossRefPubMedGoogle Scholar
  30. Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964CrossRefPubMedPubMedCentralGoogle Scholar
  31. Ma HF, Zheng XX, Peng MH, Bian H, Chen MM, Liu YQ, Jiang XF, Qin L (2016) Complete mitochondrial genome of the meadow moth, Loxostege sticticalis (Lepidoptera: Pyraloidea: Crambidae), compared to other Pyraloidea moths. J Asia-Pac Entomol 19:697–706CrossRefGoogle Scholar
  32. Macey JR, Schulte JA, Larson A, Papenfuss TJ (1998) Tandem duplication via light strand synthesis may provide a precursor for mitochondrial genomic rearrangement. Mol Biol Evol 15:71–75CrossRefPubMedGoogle Scholar
  33. Moritz C, Dowling TE, Brown WM (1987) Evolution of animal mitochondrial DNA: relevance for population biology and systematics. Annu Rev Ecol Syst 18:269–292CrossRefGoogle Scholar
  34. Nardi F, Spinsanti G, Boore JL, Carapelli A, Dallai R, Frati F (2003) Hexapod origins: monophyletic or paraphyletic? Science 299:1887–1889CrossRefPubMedGoogle Scholar
  35. Nylin S, Slove J, Janz N (2014) Host plant utilization, host range oscillations and diversification in nymphalid butterflies: a phylogenetic investigation. Evolution 68:105–124CrossRefPubMedGoogle Scholar
  36. Nymphalidae Systematics Group (2016) The subfamily Danainae. http://www.nymphalidae.net/http://www.Nymphalidae/Danainae/Danainae.htm. Accessed 20 Sept 2016
  37. Ojala D, Merkel C, Gelfand R, Attardi G (1980) The tRNA genes punctuate the reading of genetic information in human mitochondrial DNA. Cell 22:393–403CrossRefPubMedGoogle Scholar
  38. Ojala D, Montoya J, Attardi G (1981) tRNA punctuation model of RNA processing in human mitochondria. Nature 290:470–474CrossRefPubMedGoogle Scholar
  39. Ômura H, Honda K (2003) Feeding responses of adult butterflies, Nymphalis xanthomelas, Kaniska canace and Vanessa indica, to components in tree sap and rotting fruits: synergistic effects of ethanol and acetic acid on sugar responsiveness. J Insect Physiol 49:1031–1038CrossRefPubMedGoogle Scholar
  40. Ômura H, Honda K (2005) Priority of color over scent during flower visitation by adult Vanessa indica butterflies. Oecologia 142:588–596CrossRefPubMedGoogle Scholar
  41. PeÑA C, Nylin S, Wahlberg N (2011) The radiation of Satyrini butterflies (Nymphalidae: Satyrinae): a challenge for phylogenetic methods. Zool J Linn Soc 161:64–87CrossRefGoogle Scholar
  42. Perna NT, Kocher TD (1995) Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. J Mol Evol 41:353–359CrossRefPubMedGoogle Scholar
  43. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefPubMedGoogle Scholar
  44. Shen J, Cong Q, Grishin NV (2015) The complete mitochondrial genome of Papilio glaucus and its phylogenetic implications. Meta Gene 5:68–83CrossRefPubMedPubMedCentralGoogle Scholar
  45. Shi QH, Sun XY, Wang YL, Hao JS, Yang Q (2015) Morphological characters are compatible with mitogenomic data in resolving the phylogeny of nymphalid butterflies (Lepidoptera: Papilionoidea: Nymphalidae). PLoS ONE 10:e0124349CrossRefPubMedPubMedCentralGoogle Scholar
  46. Shields O (1989) World numbers of butterflies. J Lepid Soc 43:178–183Google Scholar
  47. Sivasankaran K, Mathew P, Anand S, Ceasar SA, Mariapackiam S, Ignacimuthu S (2017) Complete mitochondrial genome sequence of fruit-piercing moth Eudocima phalonia (Linnaeus, 1763) (Lepidoptera: Noctuoidea). Genom Data 14:66–81CrossRefPubMedPubMedCentralGoogle Scholar
  48. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57:758–771CrossRefPubMedGoogle Scholar
  49. Swindell SR, Plasterer TN (1997) Seqman. Contig assembly. Methods Mol Biol 70:75PubMedGoogle Scholar
  50. Taanman JW (1999) The mitochondrial genome: structure, transcription, translation and replication. Biochim Biophys Acta 1410:103–123CrossRefPubMedGoogle Scholar
  51. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefPubMedPubMedCentralGoogle Scholar
  52. Wahlberg N, Brower AVZ (2008) Nymphalinae Rafinesque 1815. The tree of life web project. http://tolweb.org/Nymphalinae/12195/2016.02.14. Accessed 14 Feb 2016
  53. Wahlberg N, Weingartner E, Nylin S (2003) Towards a better understanding of the higher systematics of Nymphalidae (Lepidoptera: Papilionoidea). Mol Phylogenet Evol 28:473–484CrossRefPubMedGoogle Scholar
  54. Wahlberg N, Leneveu J, Kodandaramaiah U, Pena C, Nylin S, Freitas AV, Brower AV (2009) Nymphalid butterflies diversify following near demise at the Cretaceous/Tertiary boundary. Proc R Soc B 276:1–8CrossRefGoogle Scholar
  55. Wolstenholme DR (1992) Animal mitochondrial DNA: structure and evolution. Int Rev Cytol 141:173–216CrossRefPubMedGoogle Scholar
  56. Yamauchi A, Nakashima T, Tokuriki N, Hosokawa M, Nogami H, Arioka S, Urabe I, Yomo T (2002) Evolvability of random polypeptides through functional selection within a small library. Protein Eng 15:619CrossRefPubMedGoogle Scholar
  57. Zhang M, Cao T, Jin K, Ren Z, Guo Y, Shi J, Zhong Y, Ma E (2008) Estimating divergence times among subfamilies in Nymphalidae. Sci Bull 53:2652–2658CrossRefGoogle Scholar
  58. Zhu BJ, Liu QN, Dai LS, Wang L, Sun Y, Lin KZ, Wei GQ, Liu CL (2013) Characterization of the complete mitochondrial genome of Diaphania pyloalis (Lepidoptera: Pyralididae). Gene 527:283–291CrossRefPubMedGoogle Scholar
  59. Zou ZW, Min Q, Cheng SY, Xin TR, Xia B (2017) The complete mitochondrial genome of Thitarodes sejilaensis (Lepidoptera: Hepialidae), a host insect of Ophiocordyceps sinensis and its implication in taxonomic revision of Hepialus adopted in China. Gene 601:44–55CrossRefPubMedGoogle Scholar

Copyright information

© The Genetics Society of Korea and Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.School of Life ScienceAnhui UniversityHefeiChina

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