Eur. J. Entomol. 114: 407-415, 2017 | DOI: 10.14411/eje.2017.052

Tandem duplication of two tRNA genes in the mitochondrial genome of Tagiades vajuna (Lepidoptera: Hesperiidae)

Fang-Fang LIU1, Yi-Ping LI1,2, Ivan JAKOVLIĆ3, Xiang-Qun YUAN1,*
1 Key Laboratory of Plant Protection Resources and Pest Management, Ministry of Education; College of Plant Protection, Northwest A&F University, Yangling, Shaanxi 712100, China; e-mails: hnndlff@163.com (F.-F.L.), lyp2003@126.com (Y.-P.L), yuanxq@nwsuaf.edu.cn (X.-Q.Y.)
2 Key Laboratory of Applied Entomology, Northwest A&F University, Yangling, Shaanxi 712100, China
3 Department of Fisheries, Beekeeping, Game Management and Special Zoology, Faculty of Agriculture, University of Zagreb, Svetošimunska cesta 25, 10000 Zagreb, Croatia; e-mail: ivanjakovlic@yahoo.com

To explore the debated phylogenetic relationship of two Hesperiidae subfamilies, Pyrginae and Eudaminae, and contribute to the understanding of the evolution of mitogenomic architecture in butterflies, we sequenced the complete mitogenome of Tagiades vajuna. The mitogenome is a typical circular duplex molecule of 15,359 bp. Apart from the standard 22 tRNAs, it has a tandem duplication of trnS(AGN) and trnE, which is unique in lepidopteran insects. Comparison with Ctenoptilum vasava indicates that the trnS1 duplication is not an ancestral state shared with other species of Tagiadini. Independent origin of the trnS1 duplications was further confirmed by the reconstruction of the ancestral character state based on the topology of the phylogram. Furthermore, comparative analysis of mitogenomes with and without tRNA duplications indicates that tRNA duplication does not alter the codon usage pattern. The mitogenome has negative AT- and GC-skews, and it is highly A+T-biased (79.7%). The AT-rich (or control) region (283 bp) contains "ATAGA" and "ATTTA" motifs. Regarding the phylogenetic analysis, we found that removal of the third codon position (3CP) from datasets used for the mitochondrial phylogenomics of Hesperiidae is likely to produce results that are more consistent: Pyrginae were rendered paraphyletic by Eudaminae in both analyses of the dataset from which the 3CP was removed (13 PCGs + all RNAs), but inclusion of the 3CP resulted in a destabilized topology, resulting in both monophyly and polyphyly. We conclude that even shallow-phylogenies of insects should pay close attention to compositional and mutational biases in mitogenomes.

Keywords: Lepidoptera, Hesperiidae, Pyrginae, Eudaminae, Tagiades vajuna, mitochondrial phylogenomics, tRNA duplication, butterflies, skippers

Received: June 21, 2017; Accepted: September 25, 2017; Revised: September 25, 2017; Published online: October 12, 2017Show citation

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LIU, F., LI, Y., JAKOVLIĆ, I., & YUAN, X. (2017). Tandem duplication of two tRNA genes in the mitochondrial genome of Tagiades vajuna (Lepidoptera: Hesperiidae). Eur. J. Entomol.114(1), 2017.000. doi: 10.14411/eje.2017.052.
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References

  1. Ballard J.W. & Whitlock M.C. 2004: The incomplete natural history of mitochondria. - Mol. Ecol. 13: 729-744. Go to original source...
  2. Bernt M., Donath A., Jühling F., Externbrink F., Florentz C., Fritzsch G., Pütz J., Middendorf M. & Stadler P.F. 2013: MITOS: Improved de novo metazoan mitochondrial genome annotation. - Mol. Phylogenet. Evol. 69: 313-319. Go to original source...
  3. Bolger A.M., Lohse M. & Usadel B. 2014: Trimmomatic: a flexible trimmer for Illumina sequence data. - Bioinformatics 30: 2114-2120. Go to original source...
  4. Brown W.M. & Wilson A.C. 1979: Rapid evolution of animal mitochondrial DNA. - Proc. Natl. Acad. Sci. U.S.A. 76: 1967-1971. Go to original source...
  5. Cameron S.L. 2014: Insect mitochondrial genomics: implications for evolution and phylogeny. - Annu. Rev. Entomol. 59: 95-117. Go to original source...
  6. Cameron S.L. & Whiting M.F. 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: 112-123. Go to original source...
  7. Cameron S.L., Lambkin C.L., Barker S.C. & Whiting M.F. 2007: A mitochondrial genome phylogeny of Diptera: whole genome sequence data accurately resolve relationships over broad timescales with high precision. - Syst. Entomol. 32: 40-59. Go to original source...
  8. Cameron S.L., Lo N., Bourguignon T., Svenson G.J. & Evans T.A. 2012: A mitochondrial genome phylogeny of termites (Blattodea: Termitoidae): robust support for interfamilial relationships and molecular synapomorphies define major clades. - Mol. Phylogenet. Evol. 65: 163-173. Go to original source...
  9. Dai L.S., Li S., Yu H.M., Wei G.Q., Wang L., Qian C., Zhang C.-F., Li J. & Sun Y. Zhao Y. 2016: Mitochondrial genome of the sweet potato hornworm, Agrius convolvuli (Lepidoptera: Sphingidae), and comparison with other Lepidoptera species. - Genome 60: 128-138. Go to original source...
  10. Doublet V., Ubrig E., Alioua A., Bouchon D., Marcadé I. & Maréchal-Drouard L. 2015: Large gene overlaps and tRNA processing in the compact mitochondrial genome of the crustacean Armadillidium vulgare. - RNA Biol. 12: 1159-1168. Go to original source...
  11. Garey J.R. & Wolstenholme D.R. 1989: Platyhelminth mitochondrial DNA: Evidence for early evolutionary origin of a tRNA ser AGN that contains a dihydrouridine arm replacement loop, and of serine-specifying AGA and AGG codons. - J. Mol. Evol. 28: 374-387. Go to original source...
  12. Gissi C., Iannelli F. & Pesole G. 2008: Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species. - Heredity 101: 301-320. Go to original source...
  13. Hahn C., Bachmann L. & Chevreux B. 2013: Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads - a baiting and iterative mapping approach. - Nucl. Acids Res. 41(13): e129, 9 pp. Go to original source...
  14. Hao J.S., Sun Q., Zhao H., Sun X., Gai Y. & Yang Q. 2012: The complete mitochondrial genome of Ctenoptilum vasava (Lepidoptera: Hesperiidae: Pyrginae) and its phylogenetic implication. - Comp. Funct. Genomics 2012(3): 328049, 13 pp. Go to original source...
  15. Hu J., Zhang D., Hao J., Huang D., Cameron S. & Zhu C. 2010: The complete mitochondrial genome of the yellow coaster, Acraea issoria (Lepidoptera: Nymphalidae: Heliconiinae: Acraeini): sequence, gene organization and a unique tRNA translocation event. - Mol. Biol. Rep. 37: 3431-3438. Go to original source...
  16. Hu F., Zhou J., Zhou L. & Tang J. 2014: Probabilistic reconstruction of ancestral gene orders with insertions and deletions. - IEEE/ACM Trans. Comput. Biol. Bioinform. 11: 667-672. Go to original source...
  17. Katoh K. & Standley D.M. 2013: MAFFT multiple sequence alignment software version 7: improvements in performance and usability. - Mol. Biol. Evol. 30: 772-780. Go to original source...
  18. Kim I., Lee E.M., Seol K.Y., Yun E.Y., Lee Y.B., Hwang J.S. & Jin B.R. 2006: The mitochondrial genome of the Korean hairstreak, Coreana raphaelis (Lepidoptera: Lycaenidae). - Insect Mol. Biol. 15: 217-225. Go to original source...
  19. Kim M.I., Baek J.Y., Kim M.J., Jeong H.C., Kim K.G., Bae C.H., Han Y.S., Jin B.R. & Kim I. 2009: Complete nucleotide sequence and organization of the mitogenome of the red-spotted apollo butterfly, Parnassius bremeri (Lepidoptera: Papilionidae) and comparison with other lepidopteran insects. - Mol. Cells 28: 347-363. Go to original source...
  20. Kim M.J., Wan X., Kim K., Hwang J.S. & Kim I. 2010: Complete nucleotide sequence and organization of the mitogenome of endangered Eumenis autonoe (Lepidoptera: Nymphalidae). - Afr. J. Biotechnol. 9: 1182-1191.
  21. Kim M.J., Kang A.R., Jeong H.C., Kim K.G. & 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: 436-445. Go to original source...
  22. Kim M.J., Wang A.R., Park J.S. & Kim I. 2014: Complete mitochondrial genomes of five skippers (Lepidoptera: Hesperiidae) and phylogenetic reconstruction of Lepidoptera. - Gene 549: 97-112. Go to original source...
  23. Lanfear R., Calcott B., Ho S.Y. & Guindon S. 2012: PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. - Mol. Biol. Evol. 29: 1695-1701. Go to original source...
  24. Li W.X., Zhang D., Boyce K., Xi B.W., Zou H., Wu S.G., Li M. & Wang G.T. 2017: The complete mitochondrial DNA of three monozoic tapeworms in the Caryophyllidea: a mitogenomic perspective on the phylogeny of eucestodes. - Parasit. Vectors 10(1): 314, 13 pp. Go to original source...
  25. Liao F., Wang L., Wu S., Li Y.-P., Zhao L., Huang G.-M., Niu C.-J., Liu Y.-Q. & Li M.-G. 2010: The complete mitochondrial genome of the fall webworm, Hyphantria cunea (Lepidoptera: Arctiidae). - Int. J. Biol. Sci. 6: 172-186. Go to original source...
  26. Min J.K., Wang A.R., Park J.S. & Kim I. 2014: Complete mitochondrial genomes of five skippers (Lepidoptera: Hesperiidae) and phylogenetic reconstruction of Lepidoptera. - Gene 549: 97-112. Go to original source...
  27. Nelson L.A., Lambkin C.L., Batterham P., Wallman J.F., Dowton M., Whiting M.F., Yeates D.K. & Cameron S.L. 2012: Beyond barcoding: A mitochondrial genomics approach to molecular phylogenetics and diagnostics of blowflies (Diptera: Calliphoridae). - Gene 511: 131-142. Go to original source...
  28. Ojala D., Montoya J. & Attardi G. 1981: tRNA punctuation model of RNA processing in human mitochondria. - Nature 290: 470-474. Go to original source...
  29. Ramírez-Ríos V., Franco-Sierra N.D., Alvarez J.C., Saldamando-Benjumea C.I. & Villanueva-Mejía D.F. 2016: Mitochondrial genome characterization of Tecia solanivora (Lepidoptera: Gelechiidae) and its phylogenetic relationship with other lepidopteran insects. - Gene 581: 107-116. Go to original source...
  30. Ratnasingham S. & Hebert P.D. 2013: A DNA-based registry for all animal species: the barcode index number (BIN) system. - PLoS One 8(7): e66213, 16 pp. Go to original source...
  31. Ronquist F., Teslenko M., Mark P.V.D., Ayres D.L., Darling A., Höhna S., Larget B., Liu L., Suchard M.A. & Huelsenbeck J.P. 2012: MrBayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. - Syst. Biol. 61: 539-542. Go to original source...
  32. Sahoo R.K., Warren A.D., Wahlberg N., Brower A.V., Lukhtanov V.A. & Kodandaramaiah U. 2016: Ten genes and two topologies: an exploration of higher relationships in skipper butterflies (Hesperiidae). - Peer J. 4: e2653, 17 pp. Go to original source...
  33. Shao L., Sun Q. & Hao J. 2015: The complete mitochondrial genome of Parara guttata (Lepidoptera: Hesperiidae). - Mitochondrial DNA 26: 724-725. Go to original source...
  34. Sheffield N.C., Song H., Cameron S.L. & Whiting M.F. 2008: A comparative analysis of mitochondrial genomes in Coleoptera (Arthropoda: Insecta) and genome descriptions of six new beetles. - Mol. Biol. Evol. 25: 2499-2509. Go to original source...
  35. Sheffield N.C., Song H., Cameron S.L. & Whiting M.F. 2009: Nonstationary evolution and compositional heterogeneity in beetle mitochondrial phylogenomics. - Syst. Biol. 58: 381-394. Go to original source...
  36. Silvestro D. & Michalak I. 2012: raxmlGUI: a graphical front-end for RAxML. - Org. Divers. Evol. 12: 335-337. Go to original source...
  37. Simon S. & Hadrys H. 2013: A comparative analysis of complete mitochondrial genomes among Hexapoda. - Mol. Phylogenet. Evol. 69: 393-403. Go to original source...
  38. Simonsen T.J., Jong R.D., Heikkilä M. & Kaila L. 2012: Butterfly morphology in a molecular age - Does it still matter in butterfly systematics? - Arthr. Struct. Dev. 41: 307-322. Go to original source...
  39. Song F., Li H., Jiang P., Zhou X., Liu J., Sun C., Vogler A.P. & Cai W. 2016: Capturing the phylogeny of Holometabola with mitochondrial genome data and Bayesian site-heterogeneous mixture models. - Genome Biol. Evol. 8: 1411-1426. Go to original source...
  40. Stamatakis A. 2014: RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. - Bioinformatics 30: 1312-1313. Go to original source...
  41. Taanman J.W. 1999: The mitochondrial genome: structure, transcription, translation and replication. - Acta Biochim. Biophys. 1410: 103-123. Go to original source...
  42. Tamura K., Stecher G., Peterson D., Filipski A. & Kumar S. 2013: MEGA6: molecular evolutionary genetics analysis version 6.0. - Mol. Biol. Evol. 30: 2725-2729. Go to original source...
  43. Wan X., Kim M.J. & Kim I. 2013: Description of new mitochondrial genomes (Spodoptera litura, Noctuoidea and Cnaphalocrocis medinalis, Pyraloidea) and phylogenetic reconstruction of Lepidoptera with the comment on optimization schemes. - Mol. Biol. Rep. 40: 6333-6349. Go to original source...
  44. Warren A.D., Ogawa J.R. & Brower A.V. 2009: Revised classification of the family Hesperiidae (Lepidoptera: Hesperioidea) based on combined molecular and morphological data. - Syst. Entomol. 34: 467-523. Go to original source...
  45. Yang X., Cameron S.L., Lees D.C., Xue D. & Han H. 2015: A mitochondrial genome phylogeny of owlet moths (Lepidoptera: Noctuoidea), and examination of the utility of mitochondrial genomes for lepidopteran phylogenetics. - Mol. Phylogenet. Evol. 85: 230-237. Go to original source...
  46. Ye F., Lan X.E., Zhu W.B. & You P. 2016: Mitochondrial genomes of praying mantises (Dictyoptera, Mantodea): rearrangement, duplication, and reassignment of tRNA genes. - Sci. Rep. 6: 25634, 9 pp. Go to original source...
  47. Yuan F., Yuan X.Q. & Xue G.X. 2015: Fauna Sinica: Insecta Vol. 55. Lepidoptera, Hesperiidae. Science Press, Beijing, 754 pp.
  48. Zhang D. 2016a: BioSuite Software. URL: https://github.com/dongzhang0725/BioSuite (last accessed 9 Oct 2016).
  49. Zhang D. 2016b: MitoTool Software. URL: https://github.com/dongzhang0725/MitoTool (last accessed 23 Oct 2016).
  50. Zhang D.X., Szymura J.M. & Hewitt G.M. 1995: Evolution and structural conservation of the control region of insect mitochondrial DNA. - J. Mol. Evol. 40: 382-391. Go to original source...
  51. Zhang D., Zou H., Wu S.G., Li M., Jakovlic I., Zhang J., Chen R., Wang G.T. & Li W.X. 2017a: Sequencing, characterization and phylogenomics of the complete mitochondrial genome of Dactylogyrus lamellatus (Monogenea: Dactylogyridae). - J. Helminthol. [in press]. Go to original source...
  52. Zhang J., Cong Q., Fan X.L., Wang R., Wang M. & Grishin N.V. 2017b: Mitogenomes of giant-skipper butterflies reveal an ancient split between deep and shallow root feeders. - F1000 Res. 6: 222, 7 pp.
  53. Zhang J., Cong Q., Shen J., Fan X.-L., Wang M. & Grishin N.V. 2017c: The complete mitogenome of Euschemon rafflesia (Lepidoptera: Hesperiidae). - Mitochondrial DNA (B) 2: 136-138. Go to original source...

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