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DNA Barcodes

Ed. by Mitchell, Andrew

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Fishing for barcodes in the Torrent: from COI to complete mitogenomes on NGS platforms

Damien D. Hinsinger
  • Institut de Systématique, Évolution, Biodiversité ISYEB, UMR 7205 CNRS, MNHN, UPMC, EPHE Muséum national d’Histoire naturelle, Sorbonne Universités. 57 rue Cuvier, CP30, 75005 Paris, France
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/ Regis Debruyne
  • Outils et Méthodes de la Systématique Intégrative, UMS 2700, MNHN, CNRS, Muséum national d’Histoire naturelle, Sorbonne Universités. 57 rue Cuvier, CP26, 75005 Paris, France
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/ Maeva Thomas
  • Unité Biologie des organismes et écosystèmes aquatiques (BOREA, UMR 7208), Sorbonne Universités, Muséum national d’Histoire naturelle, Université Pierre et Marie Curie, Université de Caen Basse-Normandie, CNRS, IRD, 57 rue Cuvier, CP26, 75005 Paris, France
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/ Gaël P. J. Denys
  • Unité Biologie des organismes et écosystèmes aquatiques (BOREA, UMR 7208), Sorbonne Universités, Muséum national d’Histoire naturelle, Université Pierre et Marie Curie, Université de Caen Basse-Normandie, CNRS, IRD, 57 rue Cuvier, CP26, 75005 Paris, France
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/ Marion Mennesson
  • Unité Biologie des organismes et écosystèmes aquatiques (BOREA, UMR 7208), Sorbonne Universités, Muséum national d’Histoire naturelle, Université Pierre et Marie Curie, Université de Caen Basse-Normandie, CNRS, IRD, 57 rue Cuvier, CP26, 75005 Paris, France
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/ Jose Utage
  • Outils et Méthodes de la Systématique Intégrative, UMS 2700, MNHN, CNRS, Muséum national d’Histoire naturelle, Sorbonne Universités. 57 rue Cuvier, CP26, 75005 Paris, France
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/ Agnes Dettai
  • Corresponding author
  • Institut de Systématique, Évolution, Biodiversité ISYEB, UMR 7205 CNRS, MNHN, UPMC, EPHE Muséum national d’Histoire naturelle, Sorbonne Universités. 57 rue Cuvier, CP30, 75005 Paris, France
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Published Online: 2015-11-26 | DOI: https://doi.org/10.1515/dna-2015-0019

Abstract

The adoption of Next-Generation Sequencing (NGS) by the field of DNA barcoding of Metazoa has been hindered by the fit between the classical COI barcode and the Sanger-based sequencing method. Here we describe a framework for the sequencing and multiplexing of mitogenomes on NGS platforms that implements (I) a universal long-range PCR-based amplification technique, (II) a two-level multiplexing approach (i.e. divergence-based and specific tag indexing), and (III) a dedicated demultiplexing and assembling script from an Ion Torrent sequencing platform. We provide a case study of mitogenomes obtained for two vouchered individuals of daces Leuciscus burdigalensis and L. oxyrrhis and show that this workflow enables to recover over 100 mitogenomes per sequencing chip on a PGM sequencer, bringing the individual cost down below 7,50€ per mitogenome (as of current 2015 sequencing costs). The use of several kilobases for identification purposes, as involved in the improved DNA-barcode we propose, stress the need for data reliability, especially through metadata. Based on both scientific and economic considerations, this framework presents a relevant approach for multiplexing samples, adaptable on any desktop NGS platform. It enables to extend from the prevalent barcoding approach by shifting from the single COI to complete mitogenome sequencing

This article offers supplementary material which is provided at the end of the article.

Keywords: DNA barcoding; mitogenome assembly; Next- Generation Sequencing; sample multiplexing; sequence post-processing

References

  • [1] Hebert P.D.N., Cywinska A., Ball S.L., deWaard J.R., Biological identifications through DNA barcodes, Proc. Biol. Sci., 2003, 270, 313-21Google Scholar

  • [2] Ward R.D., Zemlak T.S., Innes B.H., Last P.R., Hebert P.D.N., DNA barcoding Australia’s fish species, Philos. Trans. R. Soc. Lond. B Biol. Sci., 2005, 360, 1847-57Google Scholar

  • [3] Ward R.D., Hanner R., Hebert P.D.N., The campaign to DNA barcode all fishes, FISH-BOL, J. Fish Biol., 2009, 74, 329-56CrossrefGoogle Scholar

  • [4] Becker S., Hanner R., Steinke D., Five years of FISH-BOL: brief status report, Mitochondrial DNA, 2011, 22 Suppl 1, 3-9Google Scholar

  • [5] Ratnasingham S., Hebert P.D.N., BOLD: The Barcode of Life Data System (http://www.barcodinglife.org), Mol. Ecol. Notes., 2007, 7, 355-64CrossrefGoogle Scholar

  • [6] Hanner R., Data standards for BARCODE records in INSDC (BRIs). 2009. http://www.barcoding.si.edu/PDF/ Guidelines%20for%20non-CO1%20selection%20FINAL.pdfGoogle Scholar

  • [7] Strohm J.H.T., Gwiazdowski R.A., Hanner R., Mitogenome metadata: current trends and proposed standards, Mitochondrial DNA.\, 2015, 1-7CrossrefGoogle Scholar

  • [8] Garcia-Vasquez E., Perez J., Martinez J.L., Pardinas A.F., Lopez B., Karaiskou N., et al., High level of mislabeling in spanish and greek hake markets suggests the fraudulent introduction of African species, J. Agric. Food Chem., 2011, 59, 475-80CrossrefGoogle Scholar

  • [9] Von der Heyden S., Barendse J., Seebregts A.J., Matthee C.A., Misleading the masses: detection of mislabeled and substituted frozen fish products in South Africa, ICES J. Mar. Sci., 2010, 176-85Google Scholar

  • [10] Naylor G.J.P., Caira J.N., Jensen K., Rosana K.A.M., White W.T., Last P.R., A DNA sequence-based approach to the identification of shark and ray species and its implications for global elasmobranch diversity and parasitology, Bull. Am. Mus. Nat. Hist., 2012, 2012Google Scholar

  • [11] Dettai A., Adamowizc S.J., Allcock L., Arango C.P., Barnes D.K.A., Barratt I., et al., DNA barcoding and molecular systematics of the benthic and demersal organisms of the CEAMARC survey, Polar Sci., 2011, 5, 298-312CrossrefGoogle Scholar

  • [12] Pompanon F., Samadi S., Next generation sequencing for characterizing biodiversity: promises and challenges, Genetica., 2015, 143, 133-8CrossrefGoogle Scholar

  • [13] Taylor H.R., Harris W.E., An emergent science on the brink of irrelevance: a review of the past 8 years of DNA barcoding, Mol. Ecol. Resour., 2012, 12, 377-88CrossrefGoogle Scholar

  • [14] Dowton M., Meiklejohn K., Cameron S.L., Wallman J., A preliminary framework for DNA barcoding, incorporating the multispecies coalescent, Syst. Biol., 2014, 63, 639-44CrossrefGoogle Scholar

  • [15] Collins R.A., Cruickshank R.H., Known Knowns, Known Unknowns, Unknown Unknowns and Unknown Knowns in DNA Barcoding: A Comment on Dowton et al., Syst. Biol., 2014, 63, 1005-9CrossrefGoogle Scholar

  • [16] Timmermans M.J.T.N., Dodsworth S., Culverwell C.L., Bocak L., Ahrens D., Littlewood D.T.J., et al., Why barcode? High-throughput multiplex sequencing of mitochondrial genomes for molecular systematics, Nucleic Acids Res., 2010, 38, e197CrossrefGoogle Scholar

  • [17] Dettai A., Gallut C., Brouillet S., Pothier J., Lecointre G., Debruyne R., Conveniently Pre-Tagged and Pre-Packaged: Extended Molecular Identification and Metagenomics Using Complete Metazoan Mitochondrial Genomes, PLoS One, 2012, 7, e51263Google Scholar

  • [18] Tang M., Tan M., Meng G., Yang S., Su X., Liu S., et al., Multiplex sequencing of pooled mitochondrial genomes-a crucial step toward biodiversity analysis using mito-metagenomics, Nucleic Acids Res., 2014, gku917Google Scholar

  • [19] Meyer M., Stenzel U., Hofreiter M., Parallel tagged sequencing on the 454 platform, Nat. Protoc., 2008, 3, 267-78CrossrefGoogle Scholar

  • [20] Bybee S.M., Bracken-Grissom H., Haynes B.D., Hermansen R.A., Byers R.L., Clement M.J., et al., Targeted amplicon sequencing (TAS): a scalable next-gen approach to multilocus, multitaxa phylogenetics, Genome Biol. Evol., 2011, 3, 1312-23CrossrefGoogle Scholar

  • [21] Feutry P., Kyne P.M., Pillans R.D., Chen X., Naylor G.J., Grewe P.M., Mitogenomics of the Speartooth Shark challenges ten years of control region sequencing, BMC Evol. Biol., 2014, 14, 232CrossrefGoogle Scholar

  • [22] Shendure J., Ji H., Next-generation DNA sequencing, Nat. Biotechnol., 2008, 26, 1135-45CrossrefGoogle Scholar

  • [23] Pollock D.D., Eisen J.A., Doggett N.A., Cummings M.P., A case for evolutionary genomics and the comprehensive examination of sequence biodiversity, Mol. Biol. Evol., 2000, 17, 1776-88CrossrefGoogle Scholar

  • [24] Rubinstein N.D., Feldstein T., Shenkar N., Botero-Castro F., Griggio F., Mastrototaro F., et al., Deep Sequencing of Mixed Total DNA without Barcodes Allows Efficient Assembly of Highly Plastic Ascidian Mitochondrial Genomes, Genome Biol. Evol., 2013, 5, 1185-99CrossrefGoogle Scholar

  • [25] Hahn C., Bachmann L., Chevreux B., Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads-a baiting and iterative mapping approach, Nucleic Acids Res., 2013, gkt371Google Scholar

  • [26] Smith D.R., The past, present and future of mitochondrial genomics: have we sequenced enough mtDNAs?, Brief. Funct. Genomics, 2015, elv027Google Scholar

  • [27] Chang Y.S., Huang F.L., Lo T.B., The complete nucleotide sequence and gene organization of carp (Cyprinus carpio) mitochondrial genome, J. Mol. Evol., 1994, 38, 138-55CrossrefGoogle Scholar

  • [28] Miya M., Kawaguchi A., Nishida M., Mitogenomic exploration of higher teleostean phylogenies: a case study for moderate-scale evolutionary genomics with 38 newly determined complete mitochondrial DNA sequences, Mol. Biol. Evol., 2001, 18, 1993-2009Google Scholar

  • [29] Miya M., Nishida M., The mitogenomic contributions to molecular phylogenetics and evolution of fishes: a 15-year retrospect, Ichthyol Res., 2015, 62, 29-71Google Scholar

  • [30] Iwasaki W., Fukunaga T., Isagozawa R., Yamada K., Maeda Y., Satoh T.P., et al., MitoFish and MitoAnnotator: a mitochondrial genome database of fish with an accurate and automatic annotation pipeline, Mol. Biol. Evol., 2013, 30, 2531-40CrossrefGoogle Scholar

  • [31] Botero-Castro F., Delsuc F., Douzery E.J.P., Thrice better than once: quality control guidelines to validate new mitogenomes, Mitochondrial DNA, 2014 Google Scholar

  • [32] Dupuis J.R., Roe A.D., Sperling F.H., Multi-locus species delimitation in closely related animals and fungi: one marker is not enough, Mol. Ecol., 2012, 21, 4422-36CrossrefGoogle Scholar

  • [33] Papadopoulou A., Anastasiou I., Vogler A.P., Revisiting the Insect Mitochondrial Molecular Clock: The Mid-Aegean Trench Calibration, Mol. Biol. Evol., 2010, 27, 1659-72CrossrefGoogle Scholar

  • [34] Li H., Shao R., Song N., Song F., Jiang P., Li Z., et al., Higher-level phylogeny of paraneopteran insects inferred from mitochondrial genome sequences, Sci. Rep., 2015, 5Google Scholar

  • [35] Kane N., Sveinsson S., Dempewolf H., Yang JY., Zhang D., Engels J.M.M., et al., Ultra-barcoding in cacao (Theobroma spp.; Malvaceae) using whole chloroplast genomes and nuclear ribosomal DNA, Am. J. Bot., 2012, 99, 320-9CrossrefGoogle Scholar

  • [36] Thompson J.D., Higgins D.G., Gibson T.J., CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice, Nucleic Acids Res., 1994, 22, 4673-80CrossrefGoogle Scholar

  • [37] Kocher T.D., Thomas W.K., Meyer A., Edwards S.V., Pääbo S., Villablanca F.X., et al., Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers, Proc. Natl. Acad. Sci. USA, 1989, 86, 6196-200CrossrefGoogle Scholar

  • [38] Schulz M.H., Zerbino D.R., Vingron M., Birney E., Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels, Bioinforma. Oxf. Engl., 2012, 28, 1086-92CrossrefGoogle Scholar

  • [39] Luo R., Liu B., Xie Y., Li Z., Huang W., Yuan J., et al., SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler, GigaScience, 2012, 1, 18Google Scholar

  • [40] Chevreux B., Wetter T., Suhai S., Genome Sequence Assembly Using Trace Signals and Additional Sequence Information., Comput. Sci. Biol. Proc. Ger. Conf. Bioinforma, GCB 99., 1999, 45-56Google Scholar

  • [41] Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J., Basic local alignment search tool, J Mol Biol., 1990, 215, 403-10Google Scholar

  • [42] Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., et al., Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data, Bioinforma. Oxf. Engl., 2012, 28, 1647-9CrossrefGoogle Scholar

  • [43] Goecks J., Nekrutenko A., Taylor J., Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences, Genome Biol., 2010, 11, R86Google Scholar

  • [44] Kottelat M., Freyhof J., Handbook of European freshwater fishes. Publications Kottelat., Berlin: Kottelat, Cornal &Freyhof;, 2007.Google Scholar

  • [45] Winnepenninckx B., Backeljau T., De Wachter R., Extraction of high molecular weight DNA from molluscs, Trends Genet., 1993, 9, 407Google Scholar

  • [46] Geiger M.F., Herder F., Monaghan M.T., Almada V., Barbieri R., Bariche M., et al., Spatial heterogeneity in the Mediterranean Biodiversity Hotspot affects barcoding accuracy of its freshwater fishes, Mol. Ecol. Resour., 2014, 14, 1210-21CrossrefGoogle Scholar

  • [47] Edgar R.C., MUSCLE: multiple sequence alignment with high accuracy and high throughput, Nucleic Acids Res., 2004, 32, 1792-7CrossrefGoogle Scholar

  • [48] Costedoat C., Chappaz R., Barascud B., Guillard O., Gilles A., Heterogeneous colonization pattern of European Cyprinids, as highlighted by the dace complex (Teleostei: Cyprinidae), Mol. Phylogenet. Evol., 2006, 41Google Scholar

  • [49] Wang F., Niu J., Hu S., Xie P., Liu C., Li H., et al., The complete mitochondrial genome of Leuciscus idus (Cypriniformes: Cyprinidae), Mitochondrial DNA., 2014Google Scholar

  • [50] Jun G Inoue M.M., Complete mitochondrial DNA sequence of the Japanese eel Anguilla japonica, Fish. Sci., 2001, 67, 118-25Google Scholar

  • [51] Kawaguchi A., Miya M., Nishida M., Complete mitochondrial DNA sequence of Aulopus japonicus (Teleostei: Aulopiformes), a basal Eurypterygii: longer DNA sequences and higher-level relationships, Ichthyol. Res., 2001, 48, 213-23CrossrefGoogle Scholar

  • [52] Kim I.-C., Kweon H.-S., Kim Y.J., Kim C.-B., Gye M.C., Lee W.-O., et al., The complete mitochondrial genome of the javeline goby Acanthogobius hasta (Perciformes, Gobiidae) and phylogenetic considerations, Gene, 2004, 336, 147-53CrossrefGoogle Scholar

  • [53] Miya M., Nishida M., Organization of the Mitochondrial Genome of a Deep-Sea Fish, Gonostoma gracile (Teleostei: Stomiiformes): First Example of Transfer RNA Gene Rearrangements in Bony Fishes, Mar. Biotechnol. N. Y. N., 1999, 1, 416-0426CrossrefGoogle Scholar

  • [54] Poulsen J.Y., Byrkjedal I., Willassen E., Rees D., Takeshima H., Satoh T.P., et al., Mitogenomic sequences and evidence from unique gene rearrangements corroborate evolutionary relationships of myctophiformes (Neoteleostei), BMC Evol. Biol., 2013, 13, 111CrossrefGoogle Scholar

  • [55] Dohm J., Lottaz C., Borodina T., Himmelbauer H., Substantial biases in ultra-short read data sets from high-throughput DNA sequencing, Nucleic Acids Res., 2008, 36Google Scholar

  • [56] Ross M.G., Russ C., Costello M., Hollinger A., Lennon N.J., Hegarty R., et al., Characterizing and measuring bias in sequence data, Genome Biol., 2013, 14, R51Google Scholar

  • [57] Zhuang X., Cheng C.H., ND6 gene “lost” and found: evolution of mitochondrial gene rearrangement in Antarctic notothenioids, Mol. Biol. Evol., 2010, 27, 1391-403Google Scholar

  • [58] Antunes A., Ramos M.J., Discovery of a large number of previously unrecognized mitochondrial pseudogenes in fish genomes, Genomics, 2005, 86, 708-17CrossrefGoogle Scholar

  • [59] Venkatesh B., Dandona N., Brenner S., Fugu genome does not contain mitochondrial pseudogenes, Genomics, 2006, 87, 307-10CrossrefGoogle Scholar

  • [60] Hazkani-Covo E., Zeller R.M., Martin W., Molecular Poltergeists: Mitochondrial DNA Copies (numts) in Sequenced Nuclear Genomes, PLoS Genet., 2010, 6, e1000834CrossrefGoogle Scholar

  • [61] Zhang J., Hanner R., Molecular Approach to the Identification of Fish in the South China Sea, PLoS One, 2012, 7, e30621Google Scholar

  • [62] Kawahara R., Miya M., Mabuchi K., Near TJ., Nishida M., Stickleback phylogenies resolved: evidence from mitochondrial genomes and 11 nuclear genes, Mol. Phylogenet. Evol., 2009, 50, 401-4Google Scholar

  • [63] Sorenson M.D., Quinn T.W., Numts: A challenge for avian systematics and population biology, The Auk, 1998, 115, 214-21Google Scholar

  • [64] Collura R.V., Stewart C.B., Insertions and duplications of mtDNA in the nuclear genomes of Old World monkeys and hominoids, Nature, 1995, 378, 485-9CrossrefGoogle Scholar

  • [65] Sato A., O’hUigin C., Figueroa F., Grant P.R., Grant B.R., Tichy H., et al., Phylogeny of Darwin’s finches as revealed by mtDNA sequences, Proc. Natl. Acad. Sci. U. S. A., 1999, 96, 5101-6 CrossrefGoogle Scholar

  • [66] Hwang U.W., Park C.J., Yong T.S., Kim W., One-step PCR amplification of complete arthropod mitochondrial genomes, Mol. Phylogenet. Evol., 2001, 19, 345-52CrossrefGoogle Scholar

  • [67] Pons J., Bauzà-Ribot M.M., Jaume D., Juan C., Next-generation sequencing, phylogenetic signal and comparative mitogenomic analyses in Metacrangonyctidae (Amphipoda: Crustacea), BMC Genomics, 2014, 15, 566CrossrefGoogle Scholar

  • [68] Green R.E., Malaspinas A.-S., Krause J., Briggs A.W., Johnson P.L.F., Uhler C., et al., A complete Neandertal mitochondrial genome sequence determined by high-throughput sequencing, Cell, 2008, 134, 416-26CrossrefGoogle Scholar

  • [69] Tsai I., Otto T., Berriman M., Improving draft assemblies by iterative mapping and assembly of short reads to eliminate gaps, Genome Biol., 2010, 11, R41Google Scholar

  • [70] Dettai A., Lecointre G., New insights into the organization and evolution of vertebrate IRBP genes and utility of IRBP gene sequences for the phylogenetic study of the Acanthomorpha (Actinopterygii: Teleostei), Mol. Phylogenet. Evol., 2008, 48, 258-69CrossrefGoogle Scholar

  • [71] Carr S.M., Marshall H.D., Intraspecific Phylogeographic Genomics From Multiple Complete mtDNA Genomes in Atlantic Cod (Gadus morhua): Origins of the “Codmother,” Transatlantic Vicariance and Midglacial Population Expansion, Genetics, 2008, 180, 381-9CrossrefGoogle Scholar

  • [72] Dettai A., Lautredou A.-C., Bonillo C., Goimbault E., Busson F., Causse R., et al., The actinopterygian diversity of the CEAMARC cruises: Barcoding and molecular taxonomy as a multi-level tool for new findings, Deep Sea Res. Part II Top. Stud. Oceanogr., 2011, 58, 250-63CrossrefGoogle Scholar

  • [73] Rokas A., Carroll S.B., More genes or more taxa? The relative contribution of gene number and taxon number to phylogenetic accuracy, Mol. Biol. Evol., 2005, 22, 1337-44 CrossrefGoogle Scholar

  • [74] Miya M., Friedman M., Satoh T.P., Takeshima H., Sado T., Iwasaki W., et al., Evolutionary Origin of the Scombridae (Tunas and Mackerels): Members of a Paleogene Adaptive Radiation with 14 Other Pelagic Fish Families, PLoS ONE., 2013, 8, e73535Google Scholar

  • [75] April J., Mayden R.L., Hanner R.H., Bernatchez L., Genetic calibration of species diversity among North America’s freshwater fishes, Proc. Natl. Acad. Sci. U. S. A., 2011, 108, 10602-7CrossrefGoogle Scholar

  • [76] Denys G.P.J., Dettai A., Persat H., Hautecoeur M., Keith P., Morphological and molecular evidence of three species of pikes Esox spp. (Actinopterygii, Esocidae) in France, including the description of a new species, C. R. Biol., 2014, 337, 521-34Google Scholar

  • [77] Knebelsberger T., Dunz A.R., Neumann D., Geiger M.F., Molecular diversity of Germany’s freshwater fishes and lampreys assessed by DNA barcoding, Mol. Ecol. Resour., 2014Google Scholar

  • [78] Hubert N., Hanner R., Holm E., Mandrak N.E., Taylor E., Burridge M., et al., Identifying Canadian freshwater fishes through DNA barcodes, PloS One., 2008, 3, e2490Google Scholar

  • [79] Brodersen J., Seehausen O., Why evolutionary biologists should get seriously involved in ecological monitoring and applied biodiversity assessment programs, Evol. Appl., 2014, 7, 968-83CrossrefGoogle Scholar

  • [80] Padial JM., Miralles A., De la Riva I., Vences M., The integrative future of taxonomy, Front. Zool., 2010, 7, 1-16Google Scholar

  • [81] Karp P.D., What we do not know about sequence analysis and sequence databases, Bioinformatics, 1998, 14, 753-4CrossrefGoogle Scholar

  • [82] Funk D.J., Omland K.E., Species level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA, Annu. Rev. Ecol. Evol. Syst., 2003, 34, 397-423 CrossrefGoogle Scholar

About the article

Received: 2015-03-31

Accepted: 2015-09-08

Published Online: 2015-11-26

Published in Print: 2015-01-01


Citation Information: DNA Barcodes, ISSN (Online) 2299-1077, DOI: https://doi.org/10.1515/dna-2015-0019.

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