Limited performance of DNA barcoding in a diverse community of tropical butterflies

Proceedings of the Royal Society B: Biological Sciences

Volumn 274, Issue 1627, 2007, Pages 2881-2889

  Elias, Marianne ^a,f   Hill, Ryan I ^b   Willmott, Keith R ^c   Dasmahapatra, Kanchon K ^d   Brower, Andrew V Z ^e   Mallet, James ^d   Jiggins, Chris D ^f  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e MIDDLE TENNESSEE STATE UNIVERSITY   (United States)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Amazon; Biodiversity; DNA barcoding; Lepidoptera; Mimicry

Indexed keywords

CYTOCHROME C OXIDASE; DNA FRAGMENT;

BIODIVERSITY; BUTTERFLY; DNA; GENETIC VARIATION; MIMICRY; MORPHOLOGY; POPULATION SIZE; SPECIATION (BIOLOGY); TAXONOMY;

ARTICLE; BUTTERFLY; DATA ANALYSIS; DEMOGRAPHY; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC CODE; GENETIC VARIABILITY; HABITAT; MITOCHONDRION; MORPHOLOGICAL TRAIT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SPECIES IDENTIFICATION; UNINDEXED SEQUENCE;

LEPIDOPTERA; PAPILIONOIDEA;

EID: 35848941738     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2007.1035     Document Type: Article

References (70)

1. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J. H., Zhang, Z., Miller, W. & Lipman, D. J. 1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402. (doi:10.1093/nar/25.17.3389)
2. Beltrán, M. S., Jiggins, C. D., Bull, V., Linares, M., Mallet, J., McMillan, W. O. & Bermingham, E. 2002 Phylogenetic discordance at the species boundary: comparative gene genealogies among rapidly radiating Heliconius butterflies. Mol. Biol. Evol. 19, 2176-2190.
3. Blaxter, M. 2003 Molecular systematics - counting angels with DNA. Nature 421, 122-124. (doi:10.1038/421122a)
4. Brower, A. V. Z. 1994 Phylogeny of Heliconius butterflies inferred from mitochondrial DNA sequences (Lepidoptera: Nymphalidae). Mol. Phyhgenet. Evol. 3, 159-174. (doi:10.1006/mpev.1994.1018)
5. Brower, A. V. Z. 1996 A new mimetic species of Heliconius (Lepidoptera: Nymphalidae), from southeastern Colombia, as revealed by cladistic analysis of mitochondrial DNA sequences. Zool. J. Linn. Soc. 116, 317-332. (doi:10.1006/zjls.1996.0022)
6. Brower, A. V. Z. 2006 Problems with DNA barcodes for species delimitation: 'ten species' of Astraptes fulgerator reassessed (Lepidoptera: Hesperiidae). Syst. Biodiv. 4, 127-132. (doi:10.1017/S147720000500191X)
7. Brower, A. V. Z., DeSalle, R. & Vogler, A. P. 1996 Gene trees, species trees and systematics: a cladistic perspective. Annu. Rev. Ecol. Syst. 27, 423-450. (doi:10.1146/annurev.ecolsys.27.1.423)
8. Brower, A. V. Z., Freitas, A. V. L., Lee, M. M., Silva-Brandao, K. L., Whinnett, A. & Willmott, K. R. 2006 Phylogenetic relationships among the Ithomiini (Lepidoptera: Nymphalidae) inferred from one mitochondrial and two nuclear gene regions. Syst. Entomol. 31, 288-301. (doi:10.1111/j.1365-3113.2006.00321.x)
9. Brown Jr, K. S. 1984 Adult-obtained pyrrolizidine alkaloids defend ithomiine butterflies against a spider predator. Nature 309, 707-709. (doi:10.1038/309707a0)
10. Cameron, S., Rubinoff, D. & Will, K. 2006 Who will actually use DNA barcoding and what will it cost? Syst. Biol. 55, 844-847. (doi:10.1080/10635150600960079)
11. Caterino, M. S., Cho, S. & Sperling, F. A. H. 2000 The current state of insect molecular systematics: a thriving tower of Babel. Annu. Rev. Entomol. 45, 1-54. (doi:10.1146/annurev.ento.45.1.1)
12. Clare, E. L., Lim, B. K., Engstrom, M. D., Eger, J. L. & Hebert, P. D. N. 2007 DNA barcoding of Neotropical bats: species identification and discovery within Guyana. Mol. Ecol. Notes 7, 184-190. (doi:10.1111/j.1471-8286.2006.01657.x)
13. Cognato, A. I. 2006 Standard percent DNA sequence difference for insects does not predict species boundaries. J. Econ. Entomol. 99, 1037-1045.
14. Danforth, B. N., Sipes, S., Fang, J. & Brady, S. G. 2006 The history of early bee diversification based on five genes plus morphology. Proc. Natl Acad. Sci. USA 103, 15 118-15 123. (doi:10.1073/pnas.0604033103)
15. DasGupta, B., Konwar, K. M., Mǎndoiu, I.I. & Shvartsman, A. A. 2005 DNA-BAR: distinguisher selection for DNA barcoding. Bioinformatics 21, 3424-3426. (doi:10.1093/bioinformatics/bti547)
16. Dasmahapatra, K. K. & Mallet, J. 2006 DNA barcodes: recent successes and future prospects. Heredity 97, 254-255. (doi:10.1038/sj.hdy. 6800858)
17. DeSalle, R., Freedman, T., Prager, E. M. & Wilson, A. C. 1987 Tempo and mode of sequence evolution in mitochondrial DNA of Hawaiian Drosophila. J. Mol. Evol. 26, 157-164. (doi:10.1007/BF02111289)
18. DeSalle, R., Egan, M. G. & Siddall, M. 2005 The unholy trinity: taxonomy, species delimitation and DNA barcoding. Phil. Trans. R. Soc. B 360, 1905-1916. (doi:10.1098/rstb.2005.1722)
19. DeVries, P. J. 1997 The butterflies of Costa Rica and their natural history, vol. 1. Papilionidae, Pieridae, Nymphalidae. Princeton, NJ: Princeton University Press.
20. Ebach, M. C. & Holdrege, C. 2005 DNA barcoding is no substitute for taxonomy. Nature 434, 697-697. (doi:10.1038/434697b)
21. Ekrem, T., Willassen, E. & Stur, E. 2007 A comprehensive DNA sequence library is essential for identification with DNA barcodes. Mol. Phylogenet. Evol. 43, 530-542. (doi:10.1016/j.ympev.2006.11.021)
22. Elias, M., et al. 2007 Phylogenetic hypothesis, pattern of speciation and evolution of wing pattern in neotropical Napeogenes butterflies (Lepidoptera: Nymphalidae). In Seventh Int. Workshop on the Molecular Biology and Genetics of the Lepidoptera 20-26 August 2006, Orthodox Academy of Crete, Kolympari, Crete, Greece, (eds K. Iatrou & P. Couble), pp. 13-14. J. Insect Sd., 7, 29.
23. Gomez, A., Wright, P. J., Lunt, D. H., Cancino, J. M., Carvalho, G. R. & Hughes, R. N. 2007 Mating trials validate the use of DNA barcoding to reveal cryptic speciation of a marine bryozoan taxon. Proc. R. Soc. B 274, 199-207. (doi:10.1098/rspb.2006.3718)
24. Guindon, S. & Gascuel, O. 2003 A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704. doi:10.1080/10635150390235520)
25. Hajibabaei, M., Janzen, D. H., Burns, J. M., Hallwachs, W. & Hebert, P. D. N. 2006a DNA barcodes distinguish species of tropical Lepidoptera. Proc. Natl Acad. Sci. USA 103, 968-971. (doi:10.1073/pnas. 0510466103)
26. Hajibabaei, M., Singer, G. A. C. & Hickey, D. A. 2006b Benchmarking DNA barcodes: an assessment using available primate sequences. Genome 49, 851-854. (doi:10.1139/G06-025)
27. Hajibabaei, M., Singer, G. A. C., Hebert, P. D. N. & Hickey, D. A. 2007 DNA barcoding: how it complements taxonomy, molecular phylogenetics and population genetics. Trends Genet. 23, 167-172. (doi:10.1016/j.tig.2007.02.001)
28. Hebert, P. D. N. & Gregory, T. R. 2005 The promise of DNA barcoding for taxonomy. Syst. Biol. 54, 852-859. (doi:10.1080/ 10635150500354886)
29. Hebert, P. D. N., Cywinska, A., Ball, S. L. & DeWaard, J. R. 2003a Biological identifications through DNA barcodes. Proc. R. Soc. B 270, 313-321. (doi:10.1098/rspb.2002.2218)
30. Hebert, P. D. N., Ratnasingham, S. & deWaard, J. R. 2003b Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc. R. Soc. B 270, S96-S99. (doi:10.1098/rsbl.2003.0025)
31. Hebert, P. D. N., Penton, E. H., Burns, J. M., Janzen, D. H. & Hallwachs, W. 2004a Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc. Natl Acad. Sci. USA 101, 14 812-14 817. (doi:10.1073/pnas.0406166101)
32. Hebert, P. D. N., Stoeckle, M. Y., Zemlak, T. S. & Francis, C M. 20046 Identification of birds through DNA barcodes. PLoS Biol. 2, 1657-1663. (doi:10.1371/journal.pbio.0020312)
33. Hickerson, M., Meyer, C. & Moritz, C. 2006 DNA barcoding will often fail to discover new animal species over broad parameter space. Syst. Biol. 55, 729-739. (doi:10.1080/10635150600969898)
34. Huelsenbeck, J. P. & Ronquist, F. 2001 MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754-755. (doi:10.1093/bioinformatics/17.8.754)
35. Hurst, G. D. D. & Jiggins, F. M. 2005 Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc. R. Soc.B 272, 1525-1534. doi:10.1098/rspb.2005.3056)
36. Janzen, D. H., Hajibabaei, M., Burns, J. M., Hallwachs, W., Remigio, E. & Hebert, P. D. N. 2005 Wedding biodiversity inventory of a large and complex Lepidoptera fauna with DNA barcoding. Phil. Trans. R. Soc. B 1462, 1835-1846. (doi:10.1098/rstb.2005.1715)
37. Jiggins, C. D., Naisbit, R. E., Coe, R. L. & Mallet, J. 2001 Reproductive isolation caused by colour pattern mimicry. Nature 411, 302-305. (doi:10.1038/35077075)
38. Jiggins, C. D., Mallarino, R., Willmott, K. W. & Bermingham, E. 2006 The phylogenetic pattern of speciation and wing pattern change in neotropical Ithomia butterflies (Lepidoptera; Nymphalidae). Evolution 60, 1454-1466.
39. Kelly, R. P., Sarkar, I. N., Eernisse, D. J. & Desalle, R. 2007 DNA barcoding using chitons (genus Mopalia). Mol. Ecol. Notes 7, 177-183. (doi:10.1111/j.1471-8286.2006.01641.x)
40. Kerr, K. C. R., Stoeckle, M. Y., Dove, C. J., Weigt, L. A., Francis, C. M. & Hebert, P. D. N. 2007 Comprehensive DNA barcode coverage of North American birds. Mol. Ecol. Notes 7, 535-543.
41. Kumar, S., Tamura, K. & Nei, M. 2004 MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform. 5, 150-163. (doi:10.1093/bib/5.2.150)
42. Lamas, G. 2004 Ithomiinae. In Atlas of neotropical Lepidoptera. Checklist: Part 4A. Hesperioidea-Papilwnoidea (ed. J. B. Heppner), pp. 172-191. Gainesville, FL: Association for Tropical Lepidoptera/Scientific Publishers.
43. Litde, D. P. & Stevenson, D. W. 2007 A comparison of algorithms for the identification of specimens using DNA barcodes: examples from gymnosperms. Cladistics 23, 1-21. (doi:10.1111/j.1096-0031.2006.00126.x)
44. Maddison, W P. & Maddison, D. R. 1997 MACCLADE: analysis of phylogeny and character evolution. Sunderland, MA: Sinauer Associates.
45. Mallarino, R., Bermingham, E., Willmott, K. R., Whinnett, A. & Jiggins, C. D. 2005 Molecular systematics of the butterfly genus Ithomia (Lepidoptera: Ithomiinae) : a composite phylogenetic hypothesis based on seven genes. Mol. Phylogenet. EvoL 34, 625-644. (doi:10.1016/j.ympev. 2004.10.021)
46. Meier, R., Shiyang, K., Vaidya, G. & Ng, P. K. L. 2006 DNA barcoding and taxonomy in Diptera: a tale of high intraspecific variability and low identification success. Syst. Biol. 55, 715-728. (doi:10.1080/10635150600969864)
47. Meyer, C. P. & Paulay, G. 2005 DNA barcoding: error rates based on comprehensive sampling. PLoS Biol. 3, 2229-2238.
48. Monaghan, M. T., Balke, M., Pons, J. & Vogler, A. P. 2006 Beyond barcodes: complex DNA taxonomy of a south pacific island radiation. Proc. R. Soc. B 273, 887-893. (doi:10.1098/rspb.2005.3391)
49. Müller, F. 1879 Ituna and Thyridia: a remarkable case of mimicry in butterflies. Trans. Entomol. Soc. London 1879, xx-xxix.
50. Nielsen, R. & Matz, M. 2006 Statistical approaches for DNA barcoding. Syst. Biol. 55, 162-169. (doi:10.1080/10635150500431239)
51. Nylander, J. A. A. 2004 MRMODELTEST V2. Program distributed by the author. Uppsala University, Sweden: Evolutionary Biology Center.
52. Pamilo, P. & Nei, M. 1988 Relationships between gene trees and species trees. Mol. Biol. Evol. 5, 568-583.
53. Ratnasingham, S. & Hebert, P. D. N. 2007 BOLD: the Barcode of Life Data System. Mol. Ecol. Notes 7, 355-364. (http://www. barcodinglife.org)
54. Rubinoff, D. 2006 Utility of mitochondrial DNA barcodes in species conservation. Conserv. Biol. 20, 1026-1033. (doi:10.1111/j.1523- 1739.2006.00542.x)
55. Rubinoff, D, Cameron, S. & Will, K. 2006 A genomic perspective on the shortcomings of mitochondrial DNA for "barcoding" identification. J. Hered. 97, 581-594. (doi:10.1093/jhered/esl036)
56. Sarkar, I. N., Joseph, W. T., Paul, J. P., David, H. F., Bernd, S. & Rob, D. 2002 An automated phylogenetic key for classifying homeoboxes. Mol. Phylogenet. Evol. 24, 388-399. (doi:10.1016/S1055-7903(02)00259-2)
57. Savolainen, V., Cowan, R. S., Vogler, A. P., Roderick, G. K. & Lane, R. 2005 Towards writing the encyclopaedia of life: an introduction to DNA barcoding. Phil. Trans. R. Soc. B 360, 1805-1811. (doi:10.1098/rstb.2005.1730)
58. Scheffer, S. J., Lewis, M. L. & Joshi, R. C. 2006 DNA barcoding applied to invasive leafminers (Diptera: Agromyzidae) in The Philippines. Ann. Entomol. Soc. Am. 99, 204-210. (doi:10.1603/0013-8746(2006) 099[0204:DBATIL]2.0.CO;2)
59. Seifert, K. A., Samson, R. A., Dewaard, J. R., Houbraken, J., Levesque, C. A., Moncalvo, J. M., Louis-Seize, G. & Hebert, P. D. N. 2007 Prospects for fungus identification using C01 DNA barcodes, with Penicillium as a test case. Proc. Natl Acad. Sci. USA 104, 3901-3906. (doi:10.1073/pnas.0611691104)
60. Smith, M. A., Woodley, N. E., Janzen, D. H., Hallwachs, W. & Hebert, P. D. N. 2006 DNA barcodes reveal cryptic host-specificity within the presumed polyphagous members of a genus of parasitoid flies (Diptera: Tachinidae). Proc. Natl Acad. Sci. USA 103, 3657-3662. (doi:10.1073/pnas. 0511318103)
61. Smith, M. A., Wood, D. M., Janzen, D. H., Hallwachs, W. & Hebert, P. D. N. 2007 DNA barcodes affirm that 16 species of apparently generalist tropical parasitoid flies (Diptera, Tachinidae) are not all generalists. Proc. Natl Acad. Sci. USA 104, 4967-4972. (doi:10.1073/pnas.0700050104)
62. van Velzen, R., Bakker, F. T. & van Loon, J. J. A. 2007 DNA barcoding reveals hidden species diversity in Cymothoe (Nymphalidae). Proc. Neth. Entomol. Soc. Meet. 18, 95-103.
63. Wahlberg, N., Brower, A. V. Z. & Nylin, S. 2005 Phylogenetic relationships and historical biogeography of tribes and genera in the subfamily Nymphalinae (Lepidoptera: Nymphalidae). Biol. J. Linn. Soc. 86, 227-251. (doi:10.1111/j.1095-8312.2005.00531.x)
64. Wheeler, Q. D. 2005 Losing the plot: DNA "barcodes" and taxonomy. Cladistics 21, 405-407. (doi:10.1111/j.1096-0031.2005. 00075.x)
65. Whinnett, A., Zimmermann, M., Willmott, K. R., Herrera, N., Mallarino, R., Simpson, F., Joron, M., Lamas, G. & Mallet, J. 2005 Strikingly variable divergence times inferred across an Amazonian butterfly 'suture zone'. Proc. R. Soc. B 272, 2525-2533. (doi:10.1098/rspb.2005.3247)
66. Whitworth, T. L., Dawson, R. D., Magalon, H. & Baudry, E. 2007 DNA barcoding cannot reliably identify species of the blowfly genus Protocalliphora (Diptera: Calliphoridae). Proc. R. Soc. B 274, 1731-1739. (doi:10.1098/rspb.2007.0062)
67. Wiemers, M. & Fiedler, K. 2007 Does the DNA barcoding gap exist? - a case study in blue butterflies (Lepidoptera: Lycaenidae). Front. Zool. 4, 8. (doi:10.1186/1742-9994-4-8)
68. Will, K. W. & Rubinoff, D. 2004 Myth of the molecule: DNA barcodes for species cannot replace morphology for identification and classification. Cladistics 20, 47-55. (doi:10.1111/j.1096-0031.2003.00008.x)
69. Will, K. W., Mishler, B. D. & Wheeler, Q. D. 2005 The perils of DNA barcoding and the need for integrative taxonomy. Syst. Biol. 54, 844-851. (doi:10.1080/10635150500354878)
70. Willmott, K. R. & Freitas, A. V. L. 2006 Higher-level phylogeny of the Ithomiinae (Lepidoptera: Nymphalidae): classification, patterns of larval hostplant colonization and diversification. Cladistics 22, 297-368. (doi:10.1111/j.1096-0031.2006.00108.x)