CC BY 4.0 · AIMS Genet 2018; 05(01): 001-023
DOI: 10.3934/genet.2018.1.1
Research Article

Our love-hate relationship with DNA barcodes, the Y2K problem, and the search for next generation barcodes

Jeffrey M. Marcus
Department of Biological Sciences, University of Manitoba, Winnipeg, MB, Canada, R3T 2N2
› Author Affiliations

Abstract

DNA barcodes are very useful for species identification especially when identification by traditional morphological characters is difficult. However, the short mitochondrial and chloroplast barcodes currently in use often fail to distinguish between closely related species, are prone to lateral transfer, and provide inadequate phylogenetic resolution, particularly at deeper nodes. The deficiencies of short barcode identifiers are similar to the deficiencies of the short year identifiers that caused the Y2K problem in computer science. The resolution of the Y2K problem was to increase the size of the year identifiers. The performance of conventional mitochondrial COI barcodes for phylogenetics was compared with the performance of complete mitochondrial genomes and nuclear ribosomal RNA repeats obtained by genome skimming for a set of caddisfly taxa (Insect Order Trichoptera). The analysis focused on Trichoptera Family Hydropsychidae, the net-spinning caddisflies, which demonstrates many of the frustrating limitations of current barcodes. To conduct phylogenetic comparisons, complete mitochondrial genomes (15 kb each) and nuclear ribosomal repeats (9 kb each) from six caddisfly species were sequenced, assembled, and are reported for the first time. These sequences were analyzed in comparison with eight previously published trichopteran mitochondrial genomes and two triochopteran rRNA repeats, plus outgroup sequences from sister clade Lepidoptera (butterflies and moths). COI trees were not well-resolved, had low bootstrap support, and differed in topology from prior phylogenetic analyses of the Trichoptera. Phylogenetic trees based on mitochondrial genomes or rRNA repeats were well-resolved with high bootstrap support and were largely congruent with each other. Because they are easily sequenced by genome skimming, provide robust phylogenetic resolution at various phylogenetic depths, can better distinguish between closely related species, and (in the case of mitochondrial genomes), are backwards compatible with existing mitochondrial barcodes, it is proposed that mitochondrial genomes and rRNA repeats be used as next generation DNA barcodes.



Publication History

Received: 22 November 2017

Accepted: 11 January 2018

Article published online:
10 May 2021

© 2018. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Hebert PDN, Cywinska A, Ball SL. et al. Biological identifications through DNA barcodes. Proc R Soc Lond B 2003; 270: 313-321
  • 2 Folmer O, Black MB, Hoch W. et al. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Bio Biotechnol 1994; 3: 294-299
  • 3 Chen CS, Huang CT, Hseu RS. Evidence for two types of nrDNA existing in Chinese medicinal fungus Ophiocordyceps sinensis . AIMS Genetics 2017; 4: 192-201
  • 4 Lebonah DE, Dileep A, Chandrasekhar K. et al. DNA barcoding on bacteria: A review. Adv Biol 2014; 2014: 541787
  • 5 Sperling JL, Silva-Brandao KL, Brandao MM. et al. Comparison of bacterial 16S rRNA variable regions for microbiome surveys of ticks. Ticks and Tick-borne Diseases 2017;8
  • 6 de Vere N, Rich TC, Trinder SA. et al. DNA barcoding for plants. Methods Mol Biol 2015; 1245: 101-118
  • 7 Heather JM, Chain B. The sequence of sequencers: The history of sequencing DNA. Genomics 2016; 107: 1-8
  • 8 Schwaller C. ‘The millennium time bomb’ or year 2000 problem: what problem? whose problem. Time Soc 1998; 7: 105-118
  • 9 Hajibabaei M, Janzen DH, Burns JM. et al. DNA barcodes distinguish species of tropical Lepidoptera. Proc Nat Acad Sci USA 2006; 103: 968-971
  • 10 Manion M, Evan WM. The Y2K problem and professional responsibility: a retrospective analysis. Technol Soc 2000; 22: 361-387
  • 11 Kulski JK. Next-Generation Sequencing—An Overview of the History, Tools, and “Omic” Applications. Kulski JK. Next Generation Sequencing—Advances, Applications and Challenges. InTech; 2016. Available from: https://www.intechopen.com/books/next-generation-sequencing-advances-applications-and-challenges/next-generation-sequencing-an-overview-of-the-history-tools-and-omic-applications
  • 12 Ratnasingham S, Hebert PDN. BOLD: The Barcode of Life Data System (http://www.barcodinglife.org). Mol Ecol Notes 2007; 7: 355-364
  • 13 Taylor HR, Harris WE. An emergent science on the brink of irrelevance: a review of the past 8 years of DNA barcoding. Mol Ecol Resour 2012; 12: 377-388
  • 14 Moritz C, Cicero C. DNA Barcoding: Promise and Pitfalls. PLoS Biol 2004; 2: e354
  • 15 Duvernell DD, Aspinwall N. Introgression of Luxilus cornutus Mtdna into allopatric populations of Luxilus chrysocephalus (Teleostei, Cyprinidae) in Missouri and Arkansas. Mol Ecol 1995; 4: 173-181
  • 16 Good JM, Hird S, Reid N. et al. Ancient hybridization and mitochondrial capture between two species of chipmunks. Mol Ecol 2008; 17: 1313-1327
  • 17 Chambers EA, Hebert PDN. Assessing DNA barcodes for species identification in North American reptiles and amphibians in natural history collections. PLoS ONE 2016; 11: e0154363
  • 18 McCullagh BS, Marcus JM. (Submitted) When barcodes go bad: Exploring the limits of DNA barcoding with complete Junonia butterfly mitochondrial genomes Submitted to Molecular Phylogenetics and Evolution: Manuscript #MPE_2017_2019.
  • 19 Bennett RF. Technology—The Y2K problem. Science 1999; 284: 438-439
  • 20 McCullagh BS, Marcus JM. The complete mitochondrional genome of Lemon Pansy, Junonia lemonias (Lepidoptera: Nymphalidae: Nymphalinae). J Asia-Pacific Ent 2015; 18: 749-755
  • 21 Hebert PDN, Penton EH, Burns JM. et al. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator . Proc Nat Acad Sci USA 2004; 101: 14812-14817
  • 22 Janzen DH, Hallwachs W. 2005 Dynamic database for an inventory of the macrocaterpillar fauna, and its food plants and parasitoids, of Area de Conservacion Guanacaste (ACG), northwestern Costa Rica http://janzen.sas.upenn.edu
  • 23 Burns JM, Janzen DH, Hajibabaei M. et al. DNA barcodes of closely related (but morphologically and ecologically distinct) species of skipper butterflies (Hesperiidae) can differ by only one to three nucleotides. J Lepid Soc 2007; 61: 138-153
  • 24 Tavares ES, Baker AJ. Single mitochondrial gene barcodes reliably identify sister-species in diverse clades of birds. BMC Evol Biol 2008; 8: 81
  • 25 Hebert PDN, deWaard JR, Landry JF. DNA barcodes for 1/1000 of the animal kingdom. Biol Lett 2010; 6: 359-362
  • 26 Vamos EE, Elbrecht V, Leese F. Short COI markers for freshwater macroinvertebrate metabarcoding. Metabarcoding and Metagenomics 2017; 1: e14625
  • 27 Stoeckle M, Bucklin A, Knowlton N. et al. 2006 Census of Marine Life DNA Barcoding Protocol. Available from: http://wwwcoreoceanorg/Dev2Goweb?id=255158
  • 28 Meusnier I, Singer GAC, Landry JF. et al. A universal DNA mini-barcode for biodiversity analysis. BMC Genomics 2008; 9: 214
  • 29 Gemmell AP, Marcus JM. A tale of two haplotype groups: The origin and distribution of divergent New World Junonia COI haplotypes. Syst Ent 2015; 40: 532-546
  • 30 Redin D, Borgstrom E, He MX. et al. Droplet Barcode Sequencing for targeted linked-read haplotyping of single DNA molecules. Nucleic Acids Res 2017;45
  • 31 Lim J, Kim SY, Kim S. et al. BioBarcode: a general DNA barcoding database and server platform for Asian biodiversity resources. BMC Genomics 2009; 10: S8
  • 32 Bezeng BS, Davies TJ, Daru BH. et al. Ten years of barcoding at the African Centre for DNA Barcoding. Genome 2017; 60: 629-638
  • 33 Carew ME, Nichols SJ, Batovska J. et al. A DNA barcode database of Australia's freshwater macroinvertebrate fauna. Mar Freshwater Res 2017; 68: 1788-1802
  • 34 Wheeler QD. Why the phylogenetic species concept?--Elementary. J Nematol 1999; 31: 134-141
  • 35 Spooner DM. DNA barcoding will frequently fail in complicated groups: an example in wild potatoes. Am J Bot 2009; 96: 1177-1189
  • 36 DeSalle R, Egan MG, Siddall M. The unholy trinity: taxonomy, species delimitation and DNA barcoding. Phil Trans R Soc B 2005; 360: 1905-1916
  • 37 Brower AVZ. Problems with DNA barcodes for species delimitation: ‘ten species’ of Astraptes fulgerator reassessed (Lepidoptera: Hesperiidae). Syst Biodivers 2006; 4: 127-132
  • 38 Brower AVZ. Alleviating the taxonomic impediment of DNA barcoding and setting a bad precedent: names for ten species of ‘Astraptes fulgerator’ (Lepidoptera: Hesperiidae: Eudaminae) with DNA-based diagnoses. Syst Biodivers 2010; 8: 485-491
  • 39 Schmidt BC, Sperling FAH. Widespread decoupling of mtDNA variation and species integrity in Grammia tiger moths (Lepidoptera: Noctuidae). Syst Ent 2008; 33: 613-634
  • 40 Dupuis JR, Sperling FAH. Repeated reticulate evolution in North American Papilio machaon group swallowtail butterflies. PLoS ONE 2015; 10: e0141882
  • 41 Glemet H, Blier P, Bernatchez L. Geographical extent of Arctic char (Salvelinus alpinus) mtDNA introgression in brook char populations (S. fontinalis) from eastern Quebec, Canada. Mol Ecol 1998; 7: 1655-1662
  • 42 Stegemann S, Keuthe M, Greiner S. et al. Horizontal transfer of chloroplast genomes between plant species. Proc Nat Acad Sci USA 2012; 109: 2434-2438
  • 43 Wortley AH, Rudall PJ, Harris DJ. et al. How much data are needed to resolve a difficult phylogeny? Case study in Lamiales. Syst Biol 2005; 54: 697-709
  • 44 Peters MJ, Marcus JM. Taxonomy as a hypothesis: testing the status of the Bermuda buckeye butterfly Junonia coenia bergi (Lepidoptera: Nymphalidae). Syst Ent 2017; 42: 288-300
  • 45 WiesemÜller B, Rothe H. Interpretation of bootstrap values in phylogenetic analysis. Anthropol Anz 2006; 64: 161-165
  • 46 Pfeiler E, Johnson S, Markow TA. DNA barcodes and insights into the relationships and systematics of buckeye butterflies (Nymphalidae: Nymphalinae: Junonia) from the Americas. J Lepid Soc 2012; 66: 185-198
  • 47 Pfeiler E, Laclette MRL, Markow TA. Polyphyly in Urbanus and Astraptes (Hesperiidae: Eudaminae) assessed using mitochondrial DNA barcodes, with a reinstated status proposed for Achalarus . J Lepid Soc 2016; 70: 85-95
  • 48 Bock DG, Kane NC, Ebert DP. et al. Genome skimming reveals the origin of the Jerusalem Artichoke tuber crop species: neither from Jerusalem nor an artichoke. New Phytol 2014; 201: 1021-1030
  • 49 Turner B, Paun O, Munzinger J. et al. Sequencing of whole plastid genomes and nuclear ribosomal DNA of Diospyros species (Ebenaceae) endemic to New Caledonia: many species, little divergence. Ann Bot 2016; 117: 1175-1185
  • 50 Dodsworth S, Chase MW, Kelly LJ. et al. Genomic repeat abundances contain phylogenetic signal. Syst Biol 2015; 64: 112-126
  • 51 Dodsworth S, Chase MW, Sarkinen T. et al. Using genomic repeats for phylogenomics: a case study in wild tomatoes (Solanum section Lycopersicon: Solanaceae). Biol J Linn Soc 2016; 117: 96-105
  • 52 Gillett CPDT, Crampton-Platt A, Timmermans MJTN. et al. Bulk de novo mitogenome assembly from pooled total DNA elucidates the phylogeny of weevils (Coleoptera: Curculionoidea). Mol Biol Evol 2014; 31: 2223-2237
  • 53 Timmermans MJTN, Dodsworth S, Culverwell CL. et al. Why barcode? High-throughput multiplex sequencing of mitochondrial genomes for molecular systematics. Nucleic Acids Res 2010; 38: e197
  • 54 Timmermans MJTN, Lees DC, Simonsen TJ. Towards a mitogenomic phylogeny of Lepidoptera. Mol Phylogen Evol 2014; 79: 169-178
  • 55 Wu LW, Lin LH, Lees D. et al. Mitogenomic sequences effectively recover relationships within brush-footed butterflies (Lepidoptera: Nymphalidae). BMC Genomics 2014; 15: 468
  • 56 Shi QH, Sun XY, Wang YL. et al. Morphological characters are compatible with mitogenomic data in resolving the phylogeny of Nymphalid butterflies (Lepidoptera: Papilionoidea: Nymphalidae). PLOS One 2015; 10: e0124349
  • 57 Wetterstrand KA. 2018 DNA sequencing costs: Data from the NHGRI Genome Sequencing Program (GSP). Available from: http://www.genome.gov/sequencingcostsdata
  • 58 Borchers TE, Marcus JM. Genetic population structure of buckeye butterflies (Junonia) from Argentina. Syst Ent 2014; 39: 242-255
  • 59 Gemmell AP, Borchers TE, Marcus JM. Genetic population structure of buckeye butterflies (Junonia) from French Guiana, Martinique, and Guadeloupe. Psyche 2014; 2014: 1-21
  • 60 Abbasi R, Marcus JM. Color pattern evolution in Vanessa butterflies (Nymphalidae: Nymphalini): Non-eyespot characters. Evol Dev 2015; 17: 63-81
  • 61 Wallace JB. Food partitioning in net-spinning trichoptera larvae: Hydropsyche venularis, Cheumatopsyche etrona, and Maconema zebratum (Hydropsychidae). Ann Entomol Soc Am 1975; 68: 463-472
  • 62 Kjer KM, Blahnik RJ, Holzenthal RW. Phylogeny of caddisflies (Insecta, Trichoptera). Zool Scr 2002; 31: 83-91
  • 63 Ruiter DE, Boyle EE, Zhou X. DNA barcoding facilitates associations and diagnoses for Trichoptera larvae of the Churchill (Manitoba, Canada) area. BMC Ecology 2013; 13: 5
  • 64 Kjer KM, Blahnik RJ, Holzenthal RW. Phylogeny of Trichoptera (Caddisflies): Characterization of signal and noise within multiple datasets. Syst Biol 2001; 50: 781-816
  • 65 Zhou X, Frandsen PB, Holzenthal RW. et al. The Trichoptera barcode initiative: a strategy for generating a species-level Tree of Life. Phil Trans R Soc B 2016; 371: 20160025
  • 66 Peters RS, Meusemann K, Petersen M. et al. The evolutionary history of holometabolous insects inferred from transcriptome-based phylogeny and comprehensive morphological data. BMC Evol Biol 2014; 14: 52
  • 67 Abbasi R, Marcus JM. A new A-P compartment boundary and organizer in holometabolous insect wings. Sci Rep 2017; 7: 16337
  • 68 Winter WD, Miller WE. Basic Techniques for Observing and Studying Moths and Butterflies. Los Angeles, CA: The Lepidopterists' Society; 2000: 444
  • 69 Living Prairie Mitogenomics Consortium. The complete mitochondrial genome of the lesser aspen webworm moth Meroptera pravella (Insecta: Lepidoptera: Pyralidae). Mitochondrial DNA B Resour 2017; 2: 344-346
  • 70 Peirson DSJ, Marcus JM. The complete mitochondrial genome of the North American caddisfly Anabolia bimaculata (Insecta: Trichoptera: Limnephilidae). Mitochondrial DNA B Resour 2017; 2: 595-597
  • 71 Lalonde MLM, Marcus JM. The complete mitochondrial genome of the long-horned caddisfly Triaenodes tardus (Insecta: Trichoptera: Leptoceridae). Mitochondrial DNA B Resour 2017; 2: 765-767
  • 72 McCullagh BS, Wissinger SA, Marcus JM. Identifying PCR primers to facilitate molecular phylogenetics in Caddisflies (order Trichoptera). Zool Syst 2015; 40: 459-469
  • 73 Kearse M, Moir R, Wilson A. et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012; 28: 1647-1649
  • 74 Reuter JS, Mathews DH. RNAstructure: software for RNA secondary structure prediction and analysis. BMC Bioinformatics 2010; 11: 129
  • 75 Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003; 31: 3406-3415
  • 76 Wang Y, Liu X, Yang D. The first mitochondrial genome for caddisfly (Insecta: Trichoptera) with phylogenetic implications. Int J Biol Scii 2014; 10: 53-63
  • 77 Wang SQ, Zhao MJ, Li TP. Complete sequence of the 10.3 kb silkworm Attacus ricini rDNA repeat, determination of the transcriptional initiation site and functional analysis of the intergenic spacer. DNA Sequence 2003; 14: 95-101
  • 78 Linard B, Arribas P, Andujar C. et al. The mitogenome of Hydropsyche pellucidula (Hydropsychidae): First gene arrangement in the insect order Trichoptera. Mitochondrial DNA A DNA Mapp Seq Anal 2017; 28: 71-72
  • 79 Dietz L, Brand P, Eschner LM. et al. The mitochondrial genomes of the caddisflies Sericostoma personatum and Thremma gallicum (Insecta: Trichoptera). Mitochondrial DNA A DNA Mapp Seq Anal 2015; 27: 3293-3294
  • 80 Sievers F, Wilm A, Dineen D. et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 2011; 7: 539
  • 81 Kim JS, Park JS, Kim MJ. et al. Complete nucleotide sequence and organization of the mitochondrial genome of eri-silkworm, Samia cynthia ricini (Lepidoptera: Saturniidae). J Asia Pac Entomol 2012; 15: 162-173
  • 82 Swofford DL. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sunderland, Massachusetts, USA: Sinauer Associates; 2002
  • 83 Darriba D, Taboada GL, Doallo R. et al. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 2012; 9: 772
  • 84 Huelsenbeck JP, Rannala B. Phylogenetic methods come of age: Testing hypotheses in an evolutionary context. Science 1997; 276: 227-232
  • 85 Ishizuka K, Matsuo M, Nonaka M. Molecular phylogenetic analysis of Catocala moths based on the nuclear ITS2 and 28S rRNA gene sequences (Lepidoptera, Noctuidae). Tinea 2015; 23: 157-170
  • 86 Briscoe AG, Bray RA, Brabec J. et al. The mitochondrial genome and ribosomal operon of Brachycladium goliath (Digenea: Brachycladiidae) recovered from a stranded minke whale. Parasitol Int 2016; 65: 271-275
  • 87 Cameron SL. Insect Mitochondrial Genomics: Implications for Evolution and Phylogeny. Annu Rev Entomol 2014; 59: 95-117
  • 88 Geraci CJ, Zhou X, Morse JC. et al. Defining the genus Hydropsyche (Trichoptera:Hydropsychidae) based on DNA and morphological evidence. J N Amer Benthol Soc 2010; 29: 918-933
  • 89 Irwin DE. Local adaptation along smooth ecological gradients causes phylogeographic breaks and phenotypic clustering. Am Nat 2012; 180: 35-49
  • 90 Heath TA, Hedtke SM, Hillis DM. Taxon sampling and the accuracy of phylogenetic analysis. J Syst Evol 2008; 46: 239-257
  • 91 Janzen DH, Hajibabaei M, Burns JM. et al. Wedding biodiversity inventory of a large and complex Lepidoptera fauna with DNA barcoding. Phil Trans Roy Soc B 2005; 360: 1835-1845
  • 92 Jaeger CM, Dombroskie JJ, Sperling FAH. Delimitation of Phaneta taradana (Moschler 1874) and P. montanana (Walsingham 1884) (Tortricidae: Olethreutinae) in Western Canada using morphology and DNA. J Lepid Soc 2013; 67: 253-262
  • 93 Proshek B, Dupuis JR, Engberg A. et al. Genetic evaluation of the evolutionary distinctness of a federally endangered butterfly, Lange's Metalmark. BMC Evol Biol 2015;15
  • 94 Wahlberg N, Weingartner E, Warren A. et al. Timing major conflict between mitochondrial and nuclear genes in species relationships of Polygonia butterflies (Nymphalidae: Nymphalini). BMC Evol Biol 2009; 9: 92
  • 95 Kodandaramaiah U, Simonsen TJ, Bromilow S. et al. Deceptive single-locus taxonomy and phylogeography: Wolbachia-associated divergence in mitochondrial DNA is not reflected in morphology and nuclear markers in a butterfly species. Ecol Evol 2013; 3: 5167-5176
  • 96 Dodsworth S. Genome skimming for next-generation biodiversity analysis. Trends Plant Sci 2015; 20: 525-527
  • 97 Lake JA. Origin of the eukaryotic nucleus by rate-invariant analyisis of rRNA sequences. Nature 1988; 331: 184-186
  • 98 Wahlberg N, Pena C, Ahola M. et al. PCR primers for 30 novel gene regions in the nuclear genomes of Lepidoptera. Zookeys 2016; 129-141
  • 99 Maricic T, Whitten M, PÄòbo S. Multiplexed DNA sequence capture of mitochondrial genomes using PCR products. PLOS ONE 2010; 11: e14004
  • 100 Breinholt JW, Earl C, Lemmon AR. et al. Resolving relationships among the megadiverse butterflies and moths with a novel pipeline for anchored phylogenomics. Syst Biol 2017; syx048