Abstract
Taxonomic misidentification of the specimens used to obtain DNA sequences is a growing problem reported for different groups of organisms, which threatens the utility of the deposited sequences in public DNA databases. This paper provides new evidence of misidentifications in molecular DNA public databases in phytophagous mites of the Tetranychidae family belonging to the group Tetranychus (Tetranychus). Several species in this group are of economic and quarantine importance in agriculture and among them Tetranychus urticae, a highly polyphagous mite causing outbreaks in many crops worldwide, is certainly the most studied. We analyzed and evaluated the identity of 105 GenBank accessions of ITS2 rDNA and 138 COI mtDNA sequences which were deposited as T. urticae and those of 14 other taxa morphologically closely related to Tetranychus sensu stricto. In addition, ITS2 and COI sequences of 18 T. urticae samples collected for this study and identified by morphological criteria, were generated and included in the analyzed dataset. Among the deposited sequences in the GenBank database, numerous cases of apparently mistaken identities were identified in the group Tetranychus s. str., especially between T. urticae, T. cinnabarinus, T. kanzawai and T. truncatus. Unreliable sequences (misidentified or dubious) were estimated at nearly 30%. In particular the analysis supports the invalidity of the controversial species status of T. cinnabarinus. More generally, it highlights the need of using combined morphological and molecular approaches to guarantee solid species diagnostics for reliable sequence accessions in public databases.
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References
Anisimova M, Gascuel O (2006) Approximate likelihood ratio test for branchs: a fast, accurate and powerful alternative. Syst Biol 55:539–552
Baker EW, Tuttle DM (1994) A guide to the spider mites (Tetranychidae) of the United States. Indira Publishing House. West Bloomfield, MI, USA
Ben Ali Z, Boursot P, Said K, Lagnel J, Chatti N, Navajas M (2000) Comparison of ribosomal ITS regions among Androctonus spp. sorpions (Scorpionida: Buthidae) from Tunisia. J Med Entomol 37:787–790
Ben-David T, Melamed S, Gerson U, Morin S (2007) ITS2 sequences as barcodes for identifying and analyzing spider mites (Acari: Tetranychidae). Exp Appl Acarol 41:169–181
Ben-David T, Gerson U, Morin S (2009) Asymmetric reprodutive inference between two closely related spider mites: Tetranychus urticae and T. turkestani (Acari: Tetranychidae). Exp Appl Acarol 48:213–227
Bolland HR, Guitierrez J, Flechtmann CHW (1998) World catalogue of the spider mite family (Acari: Tetranychidae). Brill Academic Publishers, Leiden
Boudreaux HB (1956) Revision of the two-spotted spider mite (Acarina, Tetranychidae) complex, Tetranychus telarius (Linnaeus). Ann Entomol Soc Am 49:43–49
Boudreaux IB, Dosse G (1963a) The usefulness of new taxonomic characters in females of the genus Tetranychus Dufour (Acari: Tetranychidae). Acarologia 5:13–33
Boudreaux IB, Dosse G (1963b) Concerning the names of some common spider mites. Adv Acarol 1:350–364
Boyer SL, Baker JM, Giribet G (2007) Deep genetic divergences in Aoraki Denticulata (Arachnida, Opiliones, Cyphophthalmi): a widespread “mite harvestmen” defies DNA taxonomy. Mol Ecol 16:4999–5016
Brandenburg RL, Kennedy GG (1981) Differences in dorsal integumentary lobe densities between Tetranychus urticae Koch and Tetranychus cinnabarinus (Boisduval) (Acarina: Tetranychidae) from northeastern North Carolina. Int J Acarol 7:231–234
Breeuwer JAJ, Jacobs G (1996) Wolbachia: intracellular manipulators of mite reproduction. Exp Appl Acarol 20:421–434
Bridge PD, Spooner BM, Panchal G (2003) On the unreliability of published DNA sequences. New Phytol 160:43–48
De Boer R (1985) Reproductive barriers. In: Helle W, Sabelis MW (eds) Spider mites: their biology, natural enemies and control: World Crop Pests, vol 1B. Elsevier Science Publishers, Amsterdam, pp 193–200
De Salle R, Egan MG, Siddall M (2005) The unholy trinity: taxonomy, species delimitation and DNA barcoding. Philos Trans Royal Soc Lond B 360:1905–1916
Diéguez-Uribeondo J, Fregeneda-Grandes JM, Cerenius L, Pérez-Iniesta E, Aller-Gancedo JM, Tellería MT, Söderhäll K, Martín MP (2007) Re-evaluation of the enigmatic species complex Saprolegnia diclina — Saprolegnia parasitica based on morphological, physiological and molecular data. Fungal Genet Biol 44:585–601
Dupont LM (1979) On gene flow between Tetranychus urticae Koch, 1836 and Tetranychus cinnabarinus (Boisduval) Boudreaux, 1956 (Acari: Tetranychidae): synonymy between the two species. Entomol Exp Appl 25:97–303
Ehara S (1999) Revision of the spider mite family Tetranychidae of Japan (Acari, Prostigmata). Species Diversity 4:63–141
Flechtmann CHW, Knihinicki DK (2002) New species and new record of Tetranychus Dufour from Australia, with a key to the major groups in this genus based on females (Acari: Prostigmata: Tetranychidae). Aust J Entomol 4:118–127
Foott WH (1962) Competition between two species of mites. I. Exp Results. Can Entomol 94:365–375
Foott WH (1963) Competition between two species of mites. II. Factors Influe Intensity. Can Entomol 9:45–57
Gotoh T, Tokioka T (1996) Genetic compatibility among diapausing red, non-diapausing red and diapausing green forms of the two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae). Jap J Entomol 64:215–225
Gotoh T, Noda H, Hong XY (2003) Wolbachia distribution and cytoplasmic incompatibility based on a survey of 42 spider mite species (Acari: Tetranychidae) in Japan. Heredity 91:208–216
Gotoh T, Noda H, Ito S (2007) Cardinium symbionts cause cytoplasmic incompatibility in spider mites. Heredity 98:13–20
Guindon S, Gascuel O (2003) PhyML: a simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
Hall TA (1999) BIOEDIT: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174
Hawksworth DL (2004) “Misidentification” in fungal DNA sequence databanks. New Phytol 161:13–14
Hinomoto N, Osakabe M, Gotoh T, Takafuji A (2001) Phylogenetic analysis of green and red forms of the two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), in Japan, based on mitochondrial cytochrome oxidase subunit I sequences. Appl Entomol Zool 36:459–464
Hinomoto N, Dinh Pha T, Anh Tuan P, Thi Bao Ngoc L, Tajima R, Ohashi K, Osakabe M, Takafuji A (2007) Identification of spider mites (Acari: Tetranychidae) by DNA sequences: a case study in Northern Vietnam. Int J Acarol 33:53–60
Holst-Jensen A, Vralstad T, Schumacher T (2004) On reliability. New Phytol 161:11–13
Hugenholtz P, Huber T (2003) Chimeric 16S rDNA sequences of diverse origin are accumulating in the public databases. Int J Syst Evol Micr 53:289–293
Hurst GDD, Jiggins FM (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
Jeppson LR, Keifer HH, Baker EW (1975) Mites injurious to economic plants. University of California Press. Berkeley, CA
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide-sequences. J Mol Evol 16:111–120
Kuang HY, Cheng LS (1990) Studies on differentiation between two sibling species Tetranychus cinnabarinus (Boisduval) and T. urticae Koch. Acta Entomol Sinica 33:109–116 In Chinese
Lanave C, Preparata G, Saccone C, Serio G (1984) A new method for calculating evolutionary substitution rates. J Mol Evol 20:86–93
Li T, Chen XL, Hong XY (2009) Population genetic structure of Tetranychus urticae and its sibling species Tetranychus cinnabaribus (Acari: Tetranychidae) in China as inferred from microsatellite data. Ann Entomol Soc Am 102:674–683
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Marrelli MT, Sallum MAM, Marinotti O (2006) The second internal transcribed spacer of nuclear ribosomal DNA as a tool for Latin American anopheline taxonomy — a critical review. Mem I Oswaldo Cruz 101:817–832
Migeon A, Dorkeld F (2006) Spider Mites Web: a comprehensive database for the Tetranychidae. http://www.montpellier.inra.fr/CBGP/spmweb. Accessed April 2009
Navajas M, Boursot P (2003) Nuclear ribosomal DNA monophyly versus mitochondrial DNA polyphyly in two closely related mite species: the influence of life history and molecular drive. P Roy Soc Lond 270:S124–S127
Navajas M, Cotton D, Kreiter S, Gutierrez J (1992) Molecular approach in spider mites (Acari: Tetranychidae): preliminary data on ribosomal DNA sequences. Exp Appl Acarol 15:211–218
Navajas M, Lagnel J, Gutierrez J, Boursot P (1998) Species-wide homogeneity of nuclear ribosomal ITS2 sequences in the spider mite Tetranychus urticae contrasts with extensive mitochondrial COI polymorphism. Heredity 80:742–752
Navajas M, Tsagkarakou A, Lagnel J, Perrot-Minnot MJ (2000) Genetic differentiation in Tetranychus urticae (Acari: Tetranychidae): polymorphism, host races or sibling species? Exp Appl Acarol 24:365–376
Navajas M, Perrot-Minnot MJ, Langnel J, Migeon A, Bourse T, Cornuet JM (2002) Genetic structure of a greenhouse population of the spider mite Tetranychus urticae: spatio-temperal analysis with microsatellite markers. Insect Mol Biol 11:157–165
Navia D, Moraes GJ, Roderick G, Navajas M (2005) The invasive coconut mite, Aceria guerreronis (Acari: Eriophyidae): origin and invasion sources inferred from mitochondrial (16S) and Ribosomal (ITS) sequences. B Entomol Res 95:505–516
Nilsson RH, Ryberg M, Kristiansson E, Abarenkov K, Larsson KH, KÃμljalg U (2006) Taxonomic reliability of DNA sequences in public sequence databases: a fungal perspective. PLoS ONE 1:e59
Osakabe MH, Hirose T, Sato M (2002) Discrimination of four Japanese Tetranychus species (Acari: Tetranychidae) using PCR-RFLP of the inter-transcribed spacer region of nuclear ribosomal DNA. Appl Entomol Zool 37:399–407
Posada D (2006) ModelTest Server: a web-based tool for the statistical selection of models of nucleotide substitution online. Nucleic Acids Res 34:W701–W703 Web Server issue
Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818
Pritchard AE, Baker EW (1955) A revision of the spider mite family Tetranychidae. Memoirs Series, vol 2. San Francisco, CA
Rodriguez F, Oliver JL, Marin A, Medina JR (1990) The general stochastic model of nucleotide substitution. J Theor Biol 142:485–501
Ros VID, Breeuwer JAJ (2007) Spider mite (Acari: Tetranychidae) mitochondrial COI phylogeny reviewed: host plant relationships, phylogeography, reproductive parasites and barcoding. Exp Appl Acarol 42:239–262
Ruedas LA, Salazar-Bravo J, Dragoo JW, Yates TL (2000) The importance of being earnest: what, if anything, constitutes a “specimen examined?”. Mol Phylogenet Evol 17:129–132
Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87:651–701
Smith Meyer MKP (1974) A revision of the Tetranychidae of Africa (Acari) with a key to the genera of the world. Department of Agricultural Technical Services, Republic of South Africa. Entomol Memoir 36:1–291
Smith Meyer MKP (Smith) (1987) African Tetranychidae (Acari: Prostigmata)—with reference to the world genera. Department of Agriculture and Water Supply, Republic of South Africa. Entomol Memoir 69:1–175
Sperling FAH, Anderson GS, Hickey DA (1994) A DNA-based approach to the identification of insect species used for postmortem interval estimation. J Forensic Sci 39:418–427
Swofford DL (2003) PAUP* phylogenetic analysis using parsimony (*and other methods), Version 4. Sinauer Associates, Sunderland, MA
Takafuji A, Santoso S, Hinomoto N (2001) Host-related differences in diapause characteristics of different geographical populations of the Kanzawa spider mite, Tetranychus kanzawai Kishida (Acari: Tetranychidae), in Japan. Appl Entomol Zool 36:177–184
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Tavaré S (1986) Some probabilistic and statistical problems in the analysis of DNA sequences. In: Miura RM (ed) Some mathematical questions in biology—DNA sequence analysis, American Mathematical Society: Lectures on Mathematics in the Life Sciences, vol Vol 17. Providence, RI, pp 57–86
Thompson JD, Higgins DG, Gibson TJ (1994) Clustal-W — improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Tsagkarakou A, Navajas M, Rousset F, Pasteur N (1999) Genetic differentiation in Tetranychus urticae (Acari: Tetranychidae) from greenhouses in France. Exp Appl Acarol 23:365–378
Tuttle DM, Baker EW (1968) Spider mites of South-western United States and a revision of the family Tetranychidae. University of Arizona Press. Tucson, AR
Vilgalys R (2003) Taxonomic misidentification in public DNA databases. New Phytol 160:3–4
Xie L, Hong XY, Xue XF (2006) Population structure of the two-spotted spider mite (Acari: Tetranychidae) from China. Ann Entomol Soc Am 99:959–965
Xie L, Xie RR, Zhang KJ, Hong XY (2008) Genetic relationship between the carmine spider mite Tetranychus cinnabarinus (Boisduval) and the two-spotted mite T. urticae Koch in China based on the mtDNA COI and rDNA ITS2 sequences. Zootaxa 1726:18–32
Zhang ZQ, Jacobson RJ (2000) Using adult female morphological characters for differentiating Tetranychus urticae complex (Acari: Tetranychidae) from greenhouse tomato crops in UK. Syst Appl Acarol 5:69–76
Acknowledgments
The authors thank Marc Maraun for valuable comments on the manuscript, Alain Migeon, for help in mite collections and mite identification, Anastasia Tsagkarakou, for providing samples from Greece and Sandrine Cros-Arteil, for technical assistance in molecular techniques. Research for this paper was conduct in partial fulfillment of the requirements of the first author for a PhD degree in Animal Biology graduate program of the Institute of Biological Sciences, Department of Zoology within the scope of a double doctoral degree program of the University of Brasília, Brazil and the University of Montpellier II, France — program SIBAGHE, Specialty: EERPG, Evolution, ecology, genetic resources and paleontology. This author thanks the members of the PhD committee: Denis Bourguet, Elisabeth Fournier, George Roderick, Isabelle Olivieri and Benoît Facon for valuable discussions. This work was partially supported by CAPES, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brazil. The authors are also greateful to CNPq, Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brazil, for the fellowship. Data used in this work were (partly) produced through molecular genetic analysis technical facilities of the IFR119 «Montpellier Environnement Biodiversité» .
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de Mendonça, R.S., Navia, D., Diniz, I.R. et al. A critical review on some closely related species of Tetranychus sensu stricto (Acari: Tetranychidae) in the public DNA sequences databases. Exp Appl Acarol 55, 1–23 (2011). https://doi.org/10.1007/s10493-011-9453-5
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DOI: https://doi.org/10.1007/s10493-011-9453-5