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DNA barcodes for species delimitation in Chironomidae (Diptera): a case study on the genus Labrundinia

Published online by Cambridge University Press:  05 September 2013

Fabio Laurindo da Silva ,
Torbjørn Ekrem  and
Alaide Aparecida Fonseca-Gessner
Fabio Laurindo da Silva*
Affiliation:
Department of Hydrobiology, Laboratory of Aquatic Entomology, Federal University of São Carlos, P.O. Box 676, 13565-905, São Carlos, SP, Brazil and Department of Natural History, NTNU University Museum, Norwegian University of Science and Technology, NO-7491, Trondheim, Norway
Torbjørn Ekrem
Affiliation:
Department of Natural History, NTNU University Museum, Norwegian University of Science and Technology, NO-7491, Trondheim, Norway
Alaide Aparecida Fonseca-Gessner
Affiliation:
Department of Hydrobiology, Laboratory of Aquatic Entomology, Federal University of São Carlos, P.O. Box 676, 13565-905, São Carlos, SP, Brazil
*
1Corresponding author (e-mail: fabelha@hotmail.com).
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Abstract

In this study, we analysed the applicability of DNA barcodes for delimitation of 79 specimens of 13 species of nonbiting midges in the subfamily Tanypodinae (Diptera: Chironomidae) from São Paulo State, Brazil. Our results support DNA barcoding as an excellent tool for species identification and for solving taxonomic conflicts in genus Labrundinia. Molecular analysis of cytochrome c oxidase subunit I (COI) gene sequences yielded taxon identification trees, supporting 13 cohesive species clusters, of which three similar groups were subsequently linked to morphological variation at the larval and pupal stage. Additionally, another cluster previously described by means of morphology was linked to molecular markers. We found a distinct barcode gap, and in some species substantial interspecific pairwise divergences (up to 19.3%) were observed, which permitted identification of all analysed species. The results also indicated that barcodes can be used to associate life stages of chironomids since COI was easily amplified and sequenced from different life stages with universal barcode primers.

Résumé

Notre étude évalue l'utilité des codes à barres d'ADN pour délimiter 79 spécimens de 13 espèces de moucherons de la sous-famille des Tanypodinae (Diptera: Chironomidae) provenant de l’état de São Paulo, Brésil. Notre étude confirme l'utilisation des codes à barres d'ADN comme un excellent outil pour l'identification des espèces et la solution de problèmes taxonomiques dans genre Labrundinia. Une analyse moléculaire des séquences des gènes COI fournit des arbres d'identification des taxons, délimitant 13 groupes cohérents d'espèces, dont trois groupes similaires ont été reliés subséquemment à une variation morphologique des stades larvaires et nymphal. De plus, un autre groupe décrit antérieurement à partir de caractères morphologiques a été relié à des marqueurs moléculaires. Il existe un écart net entre les codes à barres et, chez certaines espèces, d'importantes divergences entre les espèces considérées deux par deux (jusqu’à 19,3%), ce qui a permis l'identification de toutes les espèces examinées. Nos résultats montrent aussi que les codes à barres peuvent servir à associer les différents stades de vie des chironomides, car il est facile d'amplifier et de séquencer le gène COI provenant des différents stades avec les amorces universelles des codes à barres.

Type
Systematics & Morphology
Information
The Canadian Entomologist , Volume 145 , Issue 6 , December 2013 , pp. 589 - 602
Copyright
Copyright © Entomological Society of Canada 2013 

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References

Aliabadian, M., Kaboli, M., Nijman, V., Vences, M. 2009. Molecular identification of birds: performance of distance-based DNA barcoding in three genes to delimit parapatric species. PLoS One, 4: e4119.CrossRefGoogle ScholarPubMed
Ashe, P.O'Connor, J.P. 2009. A world catalogue of Chironomidae (Diptera). Part 1. Buchonomyiinae, Chilenomyiinae, Podonominae, Aphroteniinae, Tanypodinae, Usambaromyiinae, Diamesinae, Prodiamesinae and Telmatogetoninae. The National Museum of Ireland, Dublin, Ireland.Google Scholar
Ball, S.L., Hebert, P.D.N., Burian, S.K., Webb, J.M. 2005. Biological identifications of mayflies (Ephemeroptera) using DNA barcodes. Journal of the North American Benthological Society, 24: 508–524.CrossRefGoogle Scholar
Bensasson, D., Zhang, D.X., Hartl, D.L., Hewitt, G.M. 2001. Mitochondrial pseudogenes: evolution's misplaced witnesses. Trends in Ecology and Evolution, 16: 314–321.CrossRefGoogle ScholarPubMed
Bryce, D.Hobart, A. 1972. The biology and identification of the larvae of the Chironomidae (Diptera). Entomologist's Gazette, 23: 175–217.Google Scholar
Carew, M.E., Marshall, S.E., Hoffmann, A.A. 2011. A combination of molecular and morphological approaches resolves species in the taxonomically difficult genus Procladius Skuse (Diptera: Chironomidae) despite high intra-specific morphological variation. Bulletin of Entomological Research, 101: 505–519.CrossRefGoogle ScholarPubMed
Carew, M.E., Pettigrove, V., Cox, R.L., Hoffmann, A.A. 2007. DNA identification of urban Tanytarsini chironomids (Diptera: Chironomidae). Journal of the North American Benthological Society, 26: 586–599.CrossRefGoogle Scholar
Carew, M.E., Pettigrove, V., Hoffmann, A.A. 2005. The utility of DNA markers in classical taxonomy: using cytochrome oxidase I markers to differentiate Australian Cladopelma (Diptera: Chironomidae) midges. Annals of the Entomological Society of America, 98: 587–594.CrossRefGoogle Scholar
Cranston, P.S., Hardy, N.B., Morse, G.E. 2012. A dated molecular phylogeny for the Chironomidae (Diptera). Systematic Entomology, 37: 172–188.CrossRefGoogle Scholar
DeSalle, R. 2007. Phenetic and DNA taxonomy; a comment on Waugh. Bioessays, 29: 1289–1290.CrossRefGoogle ScholarPubMed
DeSalle, R., Egan, M.G., Siddall, M.E. 2005. The unholy trinity: taxonomy, species delimitation and DNA barcoding. Proceedings of the Royal Society of London Series B: Biological Science, 360: 1905–1916.Google ScholarPubMed
Ebach, M.C. 2011. Taxonomy and the DNA barcoding enterprise. Zootaxa, 2742: 67–68.CrossRefGoogle Scholar
Ekrem, T., Stur, E., Hebert, P.D.N. 2010a. Females do count: documenting Chironomidae (Diptera) species diversity using DNA barcoding. Organisms Diversity & Evolution, 10: 397–408.CrossRefGoogle Scholar
Ekrem, T., Willassen, E., Stur, E. 2007. A comprehensive DNA library is essential for identification with DNA barcodes. Molecular Phylogenetics and Evolution, 43: 530–542.CrossRefGoogle ScholarPubMed
Ekrem, T., Willassen, E., Stur, E. 2010b. Phylogenetic utility of five genes for dipteran phylogeny: a test case in the Chironomidae leads to generic synonymies. Molecular Phylogenetics and Evolution, 57: 561–571.CrossRefGoogle ScholarPubMed
Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39: 783–791.CrossRefGoogle ScholarPubMed
Fittkau, E.J. 1962. Die Tanypodinae (Diptera: Chironomidae): Die Tribus Anatopyniini, Macropelopiini und Pentaneurini. Abhandlungen zur Larvalsystematik der Insekten, 6: 1–453.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R., Vrijenhoek, R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3: 294–299.Google ScholarPubMed
Foottit, R.G.Adler, P.H. 2009. Insect biodiversity, science and society. Wiley-Blackwell West Sussex, United Kingdom.CrossRefGoogle Scholar
Funk, D.J.Omland, K.E. 2003. Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology, Evolution, and Systematics, 34: 397–423.CrossRefGoogle Scholar
Gouin, F.J. 1959. Morphology of the larval head of some Chironomidae (Diptera, Nematocera). Smithsonian Miscellaneous Collections, 137: 175–201.Google Scholar
Hajibabaei, M., Janzen, D.H., Burns, J.M., Hallwachs, W., Hebert, P.D.N. 2006. DNA barcodes distinguish species of tropical Lepidoptera. Proceedings of the National Academy of Science, 103: 968–977.CrossRefGoogle ScholarPubMed
Hammer, Ø., Harper, D.A.T., Ryan, P.D. 2001. PAST: palaeontological statistics software package for education and data analysis. Palaeontologia Electronica, 4: 1–9.Google Scholar
Hebert, P.D.N., Cywinska, A., Ball, S.L., DeWaard, J.R. 2003. Biological identifications through DNA barcodes. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270: 313–321.CrossRefGoogle ScholarPubMed
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. Proceedings of the National Academy of Sciences, 101: 14812–14817.CrossRefGoogle ScholarPubMed
Hebert, P.D.N., Stoeckle, M.Y., Zemlak, T.S., Francis, C.M. 2004b. Identification of birds through DNA barcodes. Plos Biology, 2: 1657–1663.CrossRefGoogle ScholarPubMed
Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16: 111–120.CrossRefGoogle ScholarPubMed
Kirkendale, L.A.Meyer, C.P. 2004. Phylogeography of the Patelloida profunda group (Gastropoda: Lottidae): diversification in a dispersal-driven marine system. Molecular Ecology, 13: 2749–2762.CrossRefGoogle Scholar
Kress, W.J., Wurdack, K.J., Zimmer, E.A., Weigt, L.A., Janzen, D.H. 2005. Use of DNA barcodes to identify flowering plants. Proceedings of the National Academy of Sciences, 102: 8369–8374.CrossRefGoogle ScholarPubMed
Lanave, C., Preparata, G., Saccone, C., Serio, G. 1984. A new method for calculating evolutionary substitution rates. Journal of Molecular Evolution, 20: 86–93.CrossRefGoogle ScholarPubMed
Meyer, C.P.Paulay, G. 2005. DNA barcoding: error rates based on comprehensive sampling. PLoS Biology, 3: 2229–2238.CrossRefGoogle ScholarPubMed
Puillandre, N., Lambert, A., Brouillet, S., Achaz, G. 2011. ABGD, automatic barcode gap discovery for primary species delimitation. Molecular Ecology, 21: 1864–1877.CrossRefGoogle ScholarPubMed
Ratnasingham, S.Hebert, P.D.N. 2007. BOLD: the barcode of life data system (www.barcodinglife.org). Molecular Ecology Notes, 7: 355–364.CrossRefGoogle ScholarPubMed
Ratnasingham, S.Hebert, P.D.N. 2013. A DNA-based registry for all animal species: The Barcode Index Number (BIN) System. PLoS ONE, 8: e66213. doi:10.1371/journal.pone.0066213.CrossRefGoogle ScholarPubMed
Roback, S.S. 1987. New species of Labrundinia from Colombia (Diptera: Chironomidae: Tanypodinae). Proceedings of the Academy of Natural Sciences of Philadelphia, 139: 211–222.Google Scholar
Rubinoff, D., Cameron, S., Will, K. 2006. A genomic perspective on the shortcomings of mitochondrial DNA for “Barcoding” identification. Journal of Heredity, 97: 581–594.CrossRefGoogle ScholarPubMed
Savolainen, V., Cowan, R.S., Vogler, A.P., Roderick, G.K., Lane, R. 2005. Towards writing the encyclopedia of life: an introduction to DNA barcoding. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 360: 1805–1811.CrossRefGoogle Scholar
Silva, F.L.Fonseca-Gessner, A.A. 2009. The immature stages of Labrundinia tenata (Diptera: Chironomidae: Tanypodinae) and redescription of the male. Zoologia, 26: 541–546.CrossRefGoogle Scholar
Silva, F.L., Fonseca-Gessner, A.A., Ekrem, T. 2011. Revision of Labrundinia maculata Roback, 1971, a new junior synonym of L. longipalpis (Goetghebuer, 1921) (Diptera: Chironomidae: Tanypodinae). Aquatic Insects, 33: 293–303.CrossRefGoogle Scholar
Silva, F.L., Wiedenbrug, S., Oliveira, C.S.N., Trivinho-Strixino, S., Pepinelli, M. 2012. Two new species of Hudsonimyia Roback, 1979 (Diptera: Chironomidae: Tanypodinae) from Neotropical Region unveiled by morphology and DNA barcoding. Journal of Natural History, 46: 1615–1648.CrossRefGoogle Scholar
Sinclair, C.S.Gresens, S.E. 2008. Discrimination of Cricotopus sp. (Diptera: Chironomidae) with mitochondrial gene cytochrome oxidase I sequences. Bulletin of Entomological Research, 98: 555–563.CrossRefGoogle Scholar
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). Proceedings of the National Academy of Sciences, 103: 3657–3662.CrossRefGoogle ScholarPubMed
Stur, E.Ekrem, T. 2011. Exploring unknown life stages of Arctic Tanytarsini (Diptera: Chironomidae) with DNA barcoding. Zootaxa, 2743: 27–39.CrossRefGoogle Scholar
Tamura, K., Nei, M., Kumar, S. 2004. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proceedings of the National Academy of Sciences (USA), 101: 11030–11035.CrossRefGoogle ScholarPubMed
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. Molecular Biology and Evolution, 28: 2731–2739.CrossRefGoogle ScholarPubMed
Thienemann, A.Zavřel, J. 1916. Die Metamorphose der Tanypinen. Archiv für Hydrobiologie und Planktonkunde, 2: 566–654.Google Scholar
Thomas, M., Raharivololoniaina, L., Glaw, F., Vences, M., Vieites, D.R. 2005. Montane tadpoles in Madagascar: molecular identification and description of the larval stages of Mantidactylus elegans, Mantidactylus medacassus and Boophis laurenti from the Andringitra Massif. Copeia, 1: 174–183.CrossRefGoogle Scholar
Thompson, J.D., Plewniak, F., Poch, O. 1999. A comprehensive comparison of multiple sequence alignment programs. Nucleic Acids Research, 27: 2682–2690.CrossRefGoogle ScholarPubMed
Virgilio, M., Backeljau, T., Nevado, B., Meyer, M.D. 2010. Comparative performances of DNA barcoding across insect orders. BMC Bioinformatics, 11: 206.CrossRefGoogle ScholarPubMed
Whitworth, T.L., Dawson, R.D., Magalon, H., Baudry, E. 2007. DNA barcoding cannot reliably identify species of the blowfly genus Protocalliphora (Diptera: Calliphoridae). Proceedings of the Royal Society B: Biological Sciences, 274: 1731–1739.CrossRefGoogle ScholarPubMed
Wiedenbrug, S., Mendes, H.F., Pepinelli, M., Trivinho-Strixino, S. 2009. Review of the genus Onconeura Andersen et Sæther (Diptera: Chironomidae), with the description of four new species from Brazil. Zootaxa, 2265: 1–26.CrossRefGoogle Scholar
Will, K.P., Mishler, P.D., Wheeler, Q.D. 2005. The perils of DNA barcoding and the need for integrative taxonomy. Systematic Biology, 54: 844–851.CrossRefGoogle ScholarPubMed